Abstract
Synaptic overproduction and elimination is a regular developmental event in the mammalian brain. In the cerebral cortex, synaptic overproduction is almost exclusively correlated with glutamatergic synapses located on dendritic spines. Therefore, analysis of changes in spine density on different parts of the dendritic tree in identified classes of principal neurons could provide insight into developmental reorganization of specific microcircuits.
The activity-dependent stabilization and selective elimination of the initially overproduced synapses is a major mechanism for generating diversity of neural connections beyond their genetic determination. The largest number of overproduced synapses was found in the monkey and human cerebral cortex. The highest (exceeding adult values by two- to threefold) and most protracted overproduction (up to third decade of life) was described for associative layer IIIC pyramidal neurons in the human dorsolateral prefrontal cortex.
Therefore, the highest proportion and extraordinarily extended phase of synaptic spine overproduction is a hallmark of neural circuitry in human higher-order associative areas. This indicates that microcircuits processing the most complex human cognitive functions have the highest level of developmental plasticity. This finding is the backbone for understanding the effect of environmental impact on the development of the most complex, human-specific cognitive and emotional capacities, and on the late onset of human-specific neuropsychiatric disorders, such as autism and schizophrenia.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abbott LF, Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci 3(Suppl):1178–1183. https://doi.org/10.1038/81453
Aghajanian GK, Bloom FE (1967) The formation of synaptic junctions in developing rat brain: a quantitative electron microscopic study. Brain Res 6:716–727. https://doi.org/10.1016/0006-8993(67)90128-x
Alexander BH, Barnes HM, Trimmer E, Davidson AM, Ogola BO, Lindsey SH, Mostany R (2018) Stable density and dynamics of dendritic spines of cortical neurons across the estrous cycle while expressing differential levels of sensory-evoked plasticity. Front Mol Neurosci 11:83. https://doi.org/10.3389/fnmol.2018.00083
Alvarez VA, Sabatini BL (2007) Anatomical and physiological plasticity of dendritic spines. Annu Rev Neurosci 30:79–97. https://doi.org/10.1146/annurev.neuro.30.051606.094222
Alzu’bi A, Homman-Ludiye J, Bourne JA, Clowry GJ (2019) Thalamocortical afferents innervate the cortical subplate much earlier in development in primate than in rodent. Cereb Cortex 29:1706–1718. https://doi.org/10.1093/cercor/bhy327
Amlien IK, Fjell AM, Tamnes CK, Grydeland H, Krogsrud SK, Chaplin TA, Rosa MGP, Walhovd KB (2016) Organizing principles of human cortical development--thickness and area from 4 to 30 years: insights from comparative primate neuroanatomy. Cereb Cortex 26:257–267. https://doi.org/10.1093/cercor/bhu214
Anderson SA, Classey JD, Condé F, Lund JS, Lewis DA (1995) Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex. Neuroscience 67:7–22. https://doi.org/10.1016/0306-4522(95)00051-J
Anlar B, Atilla P, Cakar N, Tombakoglu M, Bulun A (2003) Apoptosis in the developing human brain: a preliminary study of the frontal region. Early Hum Dev 71:53–60. https://doi.org/10.1016/s0378-3782(02)00116-0
Anton-Sanchez L, Larrañaga P, Benavides-Piccione R, Fernaud-Espinosa I, DeFelipe J, Bielza C (2017) Three-dimensional spatial modeling of spines along dendritic networks in human cortical pyramidal neurons. PLoS One 12:e0180400. https://doi.org/10.1371/journal.pone.0180400
Appelbaum LG, Shenasa MA, Stolz L, Daskalakis Z (2023) Synaptic plasticity and mental health: methods, challenges and opportunities. Neuropsychopharmacology 48:113–120. https://doi.org/10.1038/s41386-022-01370-w
Arellano JI, Benavides-Piccione R, DeFelipe J, Yuste R (2007) Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front Neurosci 1:131–143. https://doi.org/10.3389/neuro.01.1.1.010.2007
Arichi T, Whitehead K, Barone G, Pressler R, Padormo F, Edwards AD, Fabrizi L (2017) Localization of spontaneous bursting neuronal activity in the preterm human brain with simultaneous EEG-fMRI. Elife 6. https://doi.org/10.7554/eLife.27814
Arion D, Corradi JP, Tang S, Datta D, Boothe F, He A, Cacace AM, Zaczek R, Albright CF, Tseng G, Lewis DA (2015) Distinctive transcriptome alterations of prefrontal pyramidal neurons in schizophrenia and schizoaffective disorder. Mol Psychiatry 20:1397–1405. https://doi.org/10.1038/mp.2014.171
Averbeck BB (2022) Pruning recurrent neural networks replicates adolescent changes in working memory and reinforcement learning. Proc Natl Acad Sci U S A 119:e2121331119. https://doi.org/10.1073/pnas.2121331119
Bączyńska E, Pels KK, Basu S, Włodarczyk J, Ruszczycki B (2021) Quantification of dendritic spines remodeling under physiological stimuli and in pathological conditions. Int J Mol Sci 22. https://doi.org/10.3390/ijms22084053
Bagust J, Lewis DM, Westerman RA (1973) Polyneuronal innervation of kitten skeletal muscle. J Physiol 229:241–255. https://doi.org/10.1113/jphysiol.1973.sp010136
Bai L, Tu WY, Xiao Y, Zhang K, Shen C (2022) Motoneurons innervation determines the distinct gene expressions in multinucleated myofibers. Cell Biosci 12:140. https://doi.org/10.1186/s13578-022-00876-6
Bakken TE, Miller JA, Ding S-L, Sunkin SM, Smith KA, Ng L, Szafer A, Dalley RA, Royall JJ, Lemon T, Shapouri S, Aiona K, Arnold J, Bennett JL, Bertagnolli D, Bickley K, Boe A, Brouner K, Butler S, Byrnes E, Caldejon S, Carey A, Cate S, Chapin M, Chen J, Dee N, Desta T, Dolbeare TA, Dotson N, Ebbert A, Fulfs E, Gee G, Gilbert TL, Goldy J, Gourley L, Gregor B, Gu G, Hall J, Haradon Z, Haynor DR, Hejazinia N, Hoerder-Suabedissen A, Howard R, Jochim J, Kinnunen M, Kriedberg A, Kuan CL, Lau C, Lee C-K, Lee F, Luong L, Mastan N, May R, Melchor J, Mosqueda N, Mott E, Ngo K, Nyhus J, Oldre A, Olson E, Parente J, Parker PD, Parry S, Pendergraft J, Potekhina L, Reding M, Riley ZL, Roberts T, Rogers B, Roll K, Rosen D, Sandman D, Sarreal M, Shapovalova N, Shi S, Sjoquist N, Sodt AJ, Townsend R, Velasquez L, Wagley U, Wakeman WB, White C, Bennett C, Wu J, Young R, Youngstrom BL, Wohnoutka P, Gibbs RA, Rogers J, Hohmann JG, Hawrylycz MJ, Hevner RF, Molnár Z, Phillips JW, Dang C, Jones AR, Amaral DG, Bernard A, Lein ES (2016) A comprehensive transcriptional map of primate brain development. Nature 535:367–375. https://doi.org/10.1038/nature18637
Balice-Gordon RJ, Lichtman JW (1994) Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372:519–524. https://doi.org/10.1038/372519a0
Balice-Gordon RJ, Thompson WJ (1988) Synaptic rearrangements and alterations in motor unit properties in neonatal rat extensor digitorum longus muscle. J Physiol 398:191–210. https://doi.org/10.1113/jphysiol.1988.sp017038
Banovac I, Sedmak D, Rojnić Kuzman M, Hladnik A, Petanjek Z (2020) Axon morphology of rapid Golgi-stained pyramidal neurons in the prefrontal cortex in schizophrenia. Croat Med J 61:354–365. https://doi.org/10.3325/cmj.2020.61.354
Barbas H (2015) General cortical and special prefrontal connections: principles from structure to function. Annu Rev Neurosci 38:269–289. https://doi.org/10.1146/annurev-neuro-071714-033936
Batiuk MY, Tyler T, Dragicevic K, Mei S, Rydbirk R, Petukhov V, Deviatiiarov R, Sedmak D, Frank E, Feher V, Habek N, Hu Q, Igolkina A, Roszik L, Pfisterer U, Garcia-Gonzalez D, Petanjek Z, Adorjan I, Kharchenko PV, Khodosevich K (2022) Upper cortical layer-driven network impairment in schizophrenia. Sci Adv 8:eabn8367. https://doi.org/10.1126/sciadv.abn8367
Becker LE, Armstrong DL, Chan F, Wood MM (1984) Dendritic development in human occipital cortical neurons. Brain Res 315:117–124. https://doi.org/10.1016/0165-3806(84)90083-X
Benavides-Piccione R, Fernaud-Espinosa I, Robles V, Yuste R, DeFelipe J (2013) Age-based comparison of human dendritic spine structure using complete three-dimensional reconstructions. Cereb Cortex 23:1798–1810. https://doi.org/10.1093/cercor/bhs154
Benavides-Piccione R, Rojo C, Kastanauskaite A, DeFelipe J (2021) Variation in pyramidal cell morphology across the human anterior temporal lobe. Cereb Cortex 31:3592–3609. https://doi.org/10.1093/cercor/bhab034
Bennett MR, Pettigrew AG (1974) The formation of synapses in striated muscle during development. J Physiol 241:515–545. https://doi.org/10.1113/jphysiol.1974.sp010670
Benoit P, Changeux JP (1975) Consequences of tenotomy on the evolution of multiinnervation in developing rat soleus muscle. Brain Res 99:354–358. https://doi.org/10.1016/0006-8993(75)90036-0
Benoit P, Changeux JP (1978) Consequences of blocking the nerve with a local anaesthetic on the evolution of multiinnervation at the regenerating neuromuscular junction of the rat. Brain Res 149:89–96. https://doi.org/10.1016/0006-8993(78)90589-9
Berg J, Sorensen SA, Ting JT, Miller JA, Chartrand T, Buchin A, Bakken TE, Budzillo A, Dee N, Ding S-L, Gouwens NW, Hodge RD, Kalmbach B, Lee C, Lee BR, Alfiler L, Baker K, Barkan E, Beller A, Berry K, Bertagnolli D, Bickley K, Bomben J, Braun T, Brouner K, Casper T, Chong P, Crichton K, Dalley R, de Frates R, Desta T, Lee SD, D’Orazi F, Dotson N, Egdorf T, Enstrom R, Farrell C, Feng D, Fong O, Furdan S, Galakhova AA, Gamlin C, Gary A, Glandon A, Goldy J, Gorham M, Goriounova NA, Gratiy S, Graybuck L, Gu H, Hadley K, Hansen N, Heistek TS, Henry AM, Heyer DB, Hill D, Hill C, Hupp M, Jarsky T, Kebede S, Keene L, Kim L, Kim M-H, Kroll M, Latimer C, Levi BP, Link KE, Mallory M, Mann R, Marshall D, Maxwell M, McGraw M, McMillen D, Melief E, Mertens EJ, Mezei L, Mihut N, Mok S, Molnar G, Mukora A, Ng L, Ngo K, Nicovich PR, Nyhus J, Olah G, Oldre A, Omstead V, Ozsvar A, Park D, Peng H, Pham T, Pom CA, Potekhina L, Rajanbabu R, Ransford S, Reid D, Rimorin C, Ruiz A, Sandman D, Sulc J, Sunkin SM, Szafer A, Szemenyei V, Thomsen ER, Tieu M, Torkelson A, Trinh J, Tung H, Wakeman W, Waleboer F, Ward K, Wilbers R, Williams G, Yao Z, Yoon J-G, Anastassiou C, Arkhipov A, Barzo P, Bernard A, Cobbs C, de Witt Hamer PC, Ellenbogen RG, Esposito L, Ferreira M, Gwinn RP, Hawrylycz MJ, Hof PR, Idema S, Jones AR, Keene CD, Ko AL, Murphy GJ, Ng L, Ojemann JG, Patel AP, Phillips JW, Silbergeld DL, Smith K, Tasic B, Yuste R, Segev I, de Kock CPJ, Mansvelder HD, Tamas G, Zeng H, Koch C, Lein ES (2021) Human neocortical expansion involves glutamatergic neuron diversification. Nature 598:151–158. https://doi.org/10.1038/s41586-021-03813-8
Berto S, Nowick K (2018) Species-specific changes in a primate transcription factor network provide insights into the molecular evolution of the primate prefrontal cortex. Genome Biol Evol 10:2023–2036. https://doi.org/10.1093/gbe/evy149
Beveridge NJ, Santarelli DM, Wang X, Tooney PA, Webster MJ, Weickert CS, Cairns MJ (2014) Maturation of the human dorsolateral prefrontal cortex coincides with a dynamic shift in microRNA expression. Schizophr Bull 40:399–409. https://doi.org/10.1093/schbul/sbs198
Bianchi S, Stimpson CD, Duka T, Larsen MD, Janssen WGM, Collins Z, Bauernfeind AL, Schapiro SJ, Baze WB, McArthur MJ, Hopkins WD, Wildman DE, Lipovich L, Kuzawa CW, Jacobs B, Hof PR, Sherwood CC (2013) Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans. Proc Natl Acad Sci U S A 110(Suppl 2):10395–10401. https://doi.org/10.1073/pnas.1301224110
Bilecki W, Maćkowiak M (2023) Gene expression and epigenetic regulation in the prefrontal cortex of schizophrenia. Genes (Basel) 14. https://doi.org/10.3390/genes14020243
Bitanihirwe BK, Woo T-UW (2021) Pyramidal neurons. In: Factors affecting neurodevelopment. Elsevier, San Diego, pp 433–445
Blakemore SJ, Mills KL (2014) Is adolescence a sensitive period for sociocultural processing? Annu Rev Psychol 65:187–207. https://doi.org/10.1146/annurev-psych-010213-115202
Blaschke AJ, Weiner JA, Chun J (1998) Programmed cell death is a universal feature of embryonic and postnatal neuroproliferative regions throughout the central nervous system. J Comp Neurol 396:39–50. https://doi.org/10.1002/(sici)1096-9861(19980622)396:1<39:aid-cne4>3.0.co;2-j
Bliss TV, Gardner-Medwin AR (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 232:357–374. https://doi.org/10.1113/jphysiol.1973.sp010274
Blundon JA, Zakharenko SS (2008) Dissecting the components of long-term potentiation. Neuroscientist 14:598–608. https://doi.org/10.1177/1073858408320643
Bock O (2013) Cajal, Golgi, Nansen, Schäfer and the neuron doctrine. Endeavour 37:228–234. https://doi.org/10.1016/j.endeavour.2013.06.006
Boivin JR, Piekarski DJ, Thomas AW, Wilbrecht L (2018) Adolescent pruning and stabilization of dendritic spines on cortical layer 5 pyramidal neurons do not depend on gonadal hormones. Dev Cogn Neurosci 30:100–107. https://doi.org/10.1016/j.dcn.2018.01.007
Bonilla-Quintana M, Wörgötter F, Tetzlaff C, Fauth M (2020) Modeling the shape of synaptic spines by their actin dynamics. Front Synaptic Neurosci 12:9. https://doi.org/10.3389/fnsyn.2020.00009
Boothe RG, Greenough WT, Lund JS, Wrege K (1979) A quantitative investigation of spine and dendrite development of neurons in visual cortex (area 17) of Macaca nemestrina monkeys. J Comp Neurol 186:473–489. https://doi.org/10.1002/cne.901860310
Borkowski WJ, Bernstine RL (1955) Electroencephalography of the fetus. Neurology 5:362–365. https://doi.org/10.1212/wnl.5.5.362
Borra E, Rizzo M, Gerbella M, Rozzi S, Luppino G (2021) Laminar origin of corticostriatal projections to the motor putamen in the macaque brain. J Neurosci 41:1455–1469. https://doi.org/10.1523/JNEUROSCI.1475-20.2020
Borra E, Biancheri D, Rizzo M, Leonardi F, Luppino G (2022) Crossed corticostriatal projections in the macaque brain. J Neurosci 42:7060–7076. https://doi.org/10.1523/JNEUROSCI.0071-22.2022
Bourgeois JP (1997) Synaptogenesis, heterochrony and epigenesis in the mammalian neocortex. Acta Paediatr Suppl 422:27–33. https://doi.org/10.1111/j.1651-2227.1997.tb18340.x
Bourgeois JP, Rakic P (1993) Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci 13:2801–2820. https://doi.org/10.1523/JNEUROSCI.13-07-02801.1993
Bourgeois JP, Rakic P (1996) Synaptogenesis in the occipital cortex of macaque monkey devoid of retinal input from early embryonic stages. Eur J Neurosci 8:942–950. https://doi.org/10.1111/j.1460-9568.1996.tb01581.x
Bourgeois JP, Jastreboff PJ, Rakic P (1989) Synaptogenesis in visual cortex of normal and preterm monkeys: evidence for intrinsic regulation of synaptic overproduction. Proc Natl Acad Sci U S A 86:4297–4301. https://doi.org/10.1073/pnas.86.11.4297
Bourgeois JP, Goldman-Rakic PS, Rakic P (1994) Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4:78–96. https://doi.org/10.1093/cercor/4.1.78
Brant AM, Munakata Y, Boomsma DI, Defries JC, Haworth CMA, Keller MC, Martin NG, McGue M, Petrill SA, Plomin R, Wadsworth SJ, Wright MJ, Hewitt JK (2013) The nature and nurture of high IQ: an extended sensitive period for intellectual development. Psychol Sci 24:1487–1495. https://doi.org/10.1177/0956797612473119
Breen MS, Ozcan S, Ramsey JM, Wang Z, Ma’ayan A, Rustogi N, Gottschalk MG, Webster MJ, Weickert CS, Buxbaum JD, Bahn S (2018) Temporal proteomic profiling of postnatal human cortical development. Transl Psychiatry 8:267. https://doi.org/10.1038/s41398-018-0306-4
Brody H (1955) Organization of the cerebral cortex. III. A study of aging in the human cerebral cortex. J Comp Neurol 102:511–516. https://doi.org/10.1002/cne.901020206
Brown MC, Jansen JK, van Essen D (1976) Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. J Physiol 261:387–422. https://doi.org/10.1113/jphysiol.1976.sp011565
Brown MC, Holland RL, Hopkins WG (1981) Restoration of focal multiple innervation in rat muscles by transmission block during a critical stage of development. J Physiol 318:355–364. https://doi.org/10.1113/jphysiol.1981.sp013869
Buffelli M, Burgess RW, Feng G, Lobe CG, Lichtman JW, Sanes JR (2003) Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424:430–434. https://doi.org/10.1038/nature01844
Burns BD (1958) The mammalian cerebral cortex. Arnold, London
Bystron I, Molnár Z, Otellin V, Blakemore C (2005) Tangential networks of precocious neurons and early axonal outgrowth in the embryonic human forebrain. J Neurosci 25:2781–2792. https://doi.org/10.1523/JNEUROSCI.4770-04.2005
Bystron I, Rakic P, Molnár Z, Blakemore C (2006) The first neurons of the human cerebral cortex. Nat Neurosci 9:880–886. https://doi.org/10.1038/nn1726
Cadwell CR, Bhaduri A, Mostajo-Radji MA, Keefe MG, Nowakowski TJ (2019) Development and arealization of the cerebral cortex. Neuron 103:980–1004. https://doi.org/10.1016/j.neuron.2019.07.009
Cajal SR (1888) Estructura de los centros nerviosos de las aves. Rev Trim Histol Norm Pat:1–10
Cajal SR (1899) Estudios sobre la cortexa cerebral humana. Estructura de la cortex motriz del hombre y mamiferos. Rev Trim Microgr 4, 117–200
Cajal SR (1904) La Textura del Sistema Nerviosa del Hombre y los Vertebrados. Moya, Madrid
Callaway EM, van Essen DC (1989) Slowing of synapse elimination by alpha-bungarotoxin superfusion of the neonatal rabbit soleus muscle. Dev Biol 131:356–365. https://doi.org/10.1016/s0012-1606(89)80009-0
Cano-Astorga N, DeFelipe J, Alonso-Nanclares L (2021) Three-dimensional synaptic organization of layer III of the human temporal neocortex. Cereb Cortex 31:4742–4764. https://doi.org/10.1093/cercor/bhab120
Caroni P, Donato F, Muller D (2012) Structural plasticity upon learning: regulation and functions. Nat Rev Neurosci 13:478–490. https://doi.org/10.1038/nrn3258
Caroni P, Chowdhury A, Lahr M (2014) Synapse rearrangements upon learning: from divergent-sparse connectivity to dedicated sub-circuits. Trends Neurosci 37:604–614. https://doi.org/10.1016/j.tins.2014.08.011
Carroll L, Braeutigam S, Dawes JM, Krsnik Z, Kostovic I, Coutinho E, Dewing JM, Horton CA, Gomez-Nicola D, Menassa DA (2021) Autism spectrum disorders: multiple routes to, and multiple consequences of, abnormal synaptic function and connectivity. Neuroscientist 27:10–29. https://doi.org/10.1177/1073858420921378
Castillo-Fernández S, Silva-Gómez AB (2022) Changes in dendritic arborization related to the estrous cycle in pyramidal neurons of layer V of the motor cortex. J Chem Neuroanat 119:102042. https://doi.org/10.1016/j.jchemneu.2021.102042
Chailangkarn T, Trujillo CA, Freitas BC, Hrvoj-Mihic B, Herai RH, Yu DX, Brown TT, Marchetto MC, Bardy C, McHenry L, Stefanacci L, Järvinen A, Searcy YM, DeWitt M, Wong W, Lai P, Ard MC, Hanson KL, Romero S, Jacobs B, Dale AM, Dai L, Korenberg JR, Gage FH, Bellugi U, Halgren E, Semendeferi K, Muotri AR (2016) A human neurodevelopmental model for Williams syndrome. Nature 536:338–343. https://doi.org/10.1038/nature19067
Chalupa LM, Killackey HP (1989) Process elimination underlies ontogenetic change in the distribution of callosal projection neurons in the postcentral gyrus of the fetal rhesus monkey. Proc Natl Acad Sci U S A 86:1076–1079. https://doi.org/10.1073/pnas.86.3.1076
Chan WY, Lorke DE, Tiu SC, Yew DT (2002) Proliferation and apoptosis in the developing human neocortex. Anat Rec 267:261–276. https://doi.org/10.1002/ar.10100
Chandrasekaran S, Navlakha S, Audette NJ, McCreary DD, Suhan J, Bar-Joseph Z, Barth AL (2015) Unbiased, high-throughput electron microscopy analysis of experience-dependent synaptic changes in the neocortex. J Neurosci 35:16450–16462. https://doi.org/10.1523/JNEUROSCI.1573-15.2015
Changeux JP (1983) L’homme neuronal. Le Temps des sciences, Fayard, Paris
Changeux JP (2017) Climbing brain levels of organisation from genes to consciousness. Trends Cogn Sci 21:168–181. https://doi.org/10.1016/j.tics.2017.01.004
Changeux JP, Danchin A (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264:705–712. https://doi.org/10.1038/264705a0
Changeux JP, Courrège P, Danchin A (1973) A theory of the epigenesis of neuronal networks by selective stabilization of synapses. Proc Natl Acad Sci U S A 70:2974–2978. https://doi.org/10.1073/pnas.70.10.2974
Changeux JP, Goulas A, Hilgetag CC (2021) A connectomic hypothesis for the hominization of the brain. Cereb Cortex 31:2425–2449. https://doi.org/10.1093/cercor/bhaa365
Charvet CJ, Finlay BL (2012) Embracing covariation in brain evolution: large brains, extended development, and flexible primate social systems. Prog Brain Res 195:71–87. https://doi.org/10.1016/B978-0-444-53860-4.00004-0
Cheetham CEJ, Barnes SJ, Albieri G, Knott GW, Finnerty GT (2014) Pansynaptic enlargement at adult cortical connections strengthened by experience. Cereb Cortex 24:521–531. https://doi.org/10.1093/cercor/bhs334
Chen CC, Brumberg JC (2021) Sensory experience as a regulator of structural plasticity in the developing Whisker-to-Barrel system. Front Cell Neurosci 15:770453. https://doi.org/10.3389/fncel.2021.770453
Chen M, Qi J, Poo M, Yang Y (2022) Stability and dynamics of dendritic spines in macaque prefrontal cortex. Natl Sci Rev 9:nwac125. https://doi.org/10.1093/nsr/nwac125
Cheour-Luhtanen M, Alho K, Sainio K, Rinne T, Reinikainen K, Pohjavuori M, Renlund M, Aaltonen O, Eerola O, Näätänen R (1996) The ontogenetically earliest discriminative response of the human brain. Psychophysiology 33:478–481. https://doi.org/10.1111/j.1469-8986.1996.tb01074.x
Chéreau R, Williams LE, Bawa T, Holtmaat A (2022) Circuit mechanisms for cortical plasticity and learning. Semin Cell Dev Biol 125:68–75. https://doi.org/10.1016/j.semcdb.2021.07.012
Chidambaram SB, Rathipriya AG, Bolla SR, Bhat A, Ray B, Mahalakshmi AM, Manivasagam T, Thenmozhi AJ, Essa MM, Guillemin GJ, Chandra R, Sakharkar MK (2019) Dendritic spines: revisiting the physiological role. Prog Neuro-Psychopharmacol Biol Psychiatry 92:161–193. https://doi.org/10.1016/j.pnpbp.2019.01.005
Chugani HT (1998) A critical period of brain development: studies of cerebral glucose utilization with PET. Prev Med 27:184–188. https://doi.org/10.1006/pmed.1998.0274
Chugani HT, Phelps ME (1986) Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. Science 231:840–843. https://doi.org/10.1126/science.3945811
Chugani HT, Phelps ME, Mazziotta JC (1987) Positron emission tomography study of human brain functional development. Ann Neurol 22:487–497. https://doi.org/10.1002/ana.410220408
Chung DW, Wills ZP, Fish KN, Lewis DA (2017) Developmental pruning of excitatory synaptic inputs to parvalbumin interneurons in monkey prefrontal cortex. Proc Natl Acad Sci U S A 114:E629–E637. https://doi.org/10.1073/pnas.1610077114
Citri A, Malenka RC (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33:18–41. https://doi.org/10.1038/sj.npp.1301559
Cline HT, Lau M, Hiramoto M (2023) Activity-dependent organization of topographic neural circuits. Neuroscience 508:3–18. https://doi.org/10.1016/j.neuroscience.2022.11.032
Collingridge GL, Peineau S, Howland JG, Wang YT (2010) Long-term depression in the CNS. Nat Rev Neurosci 11:459–473. https://doi.org/10.1038/nrn2867
Conradi S, Ronnevi LO (1975) Spontaneous elimination of synapses on cat spinal motoneurons after birth: do half of the synapses on the cell bodies disappear? Brain Res 92:505–510. https://doi.org/10.1016/0006-8993(75)90338-8
Conradi S, Skoglund S (1969) Observations on the ultrastructure of the initial motor axon segment and dorsal root boutons on the motoneurons in the lumbosacral spinal cord of the cat during postnatal development. Acta Physiol Scand Suppl 333:53–76
Cragg BG (1975) The development of synapses in the visual system of the cat. J Comp Neurol 160:147–166. https://doi.org/10.1002/cne.901600202
Crepel F, Mariani J, Delhaye-Bouchaud N (1976) Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J Neurobiol 7:567–578. https://doi.org/10.1002/neu.480070609
Dall’Orso S, Arichi T, Fitzgibbon SP, Edwards AD, Burdet E, Muceli S (2022) Development of functional organization within the sensorimotor network across the perinatal period. Hum Brain Mapp 43:2249–2261. https://doi.org/10.1002/hbm.25785
Datta D, Arnsten AFT (2018) Unique molecular regulation of higher-order prefrontal cortical circuits: insights into the neurobiology of schizophrenia. ACS Chem Neurosci 9:2127–2145. https://doi.org/10.1021/acschemneuro.7b00505
Daw NW, Fox K, Sato H, Czepita D (1992) Critical period for monocular deprivation in the cat visual cortex. J Neurophysiol 67:197–202. https://doi.org/10.1152/jn.1992.67.1.197
Dawkins R (1971) Selective neurone death as a possible memory mechanism. Nature 229:118–119. https://doi.org/10.1038/229118a0
de Asis-Cruz J, Barnett SD, Kim J-H, Limperopoulos C (2021) Functional connectivity-derived optimal gestational-age cut points for fetal brain network maturity. Brain Sci 11. https://doi.org/10.3390/brainsci11070921
de Robertis ED, Bennett HS (1955) Some features of the submicroscopic morphology of synapses in frog and earthworm. J Biophys Biochem Cytol 1:47–58. https://doi.org/10.1083/jcb.1.1.47
de Roo M, Klauser P, Muller D (2008) LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol 6:e219. https://doi.org/10.1371/journal.pbio.0060219
Dehay C, Kennedy H, Bullier J, Berland M (1988) Absence of interhemispheric connections of area 17 during development in the monkey. Nature 331:348–350. https://doi.org/10.1038/331348a0
Delevich K, Okada NJ, Rahane A, Zhang Z, Hall CD, Wilbrecht L (2020) Sex and pubertal status influence dendritic spine density on frontal corticostriatal projection neurons in mice. Cereb Cortex 30:3543–3557. https://doi.org/10.1093/cercor/bhz325
Derbyshire SW, Bockmann JC (2020) Reconsidering fetal pain. J Med Ethics 46:3–6. https://doi.org/10.1136/medethics-2019-105701
Di Maio V (2021) The glutamatergic synapse: a complex machinery for information processing. Cogn Neurodyn 15:757–781. https://doi.org/10.1007/s11571-021-09679-w
Dienel SJ, Bazmi HH, Lewis DA (2017) Development of transcripts regulating dendritic spines in layer 3 pyramidal cells of the monkey prefrontal cortex: implications for the pathogenesis of schizophrenia. Neurobiol Dis 105:132–141. https://doi.org/10.1016/j.nbd.2017.05.016
Dienel SJ, Schoonover KE, Lewis DA (2022) Cognitive dysfunction and prefrontal cortical circuit alterations in schizophrenia: developmental trajectories. Biol Psychiatry 92:450–459. https://doi.org/10.1016/j.biopsych.2022.03.002
Ding SL, Royall JJ, Lesnar P, Facer BAC, Smith KA, Wei Y, Brouner K, Dalley RA, Dee N, Dolbeare TA, Ebbert A, Glass IA, Keller NH, Lee F, Lemon TA, Nyhus J, Pendergraft J, Reid R, Sarreal M, Shapovalova NV, Szafer A, Phillips JW, Sunkin SM, Hohmann JG, Jones AR, Hawrylycz MJ, Hof PR, Ng L, Bernard A, Lein ES (2022) Cellular resolution anatomical and molecular atlases for prenatal human brains. J Comp Neurol 530:6–503. https://doi.org/10.1002/cne.25243
Diniz CRAF, Crestani AP (2023) The times they are a-changin’: a proposal on how brain flexibility goes beyond the obvious to include the concepts of “upward” and “downward” to neuroplasticity. Mol Psychiatry 28:977–992. https://doi.org/10.1038/s41380-022-01931-x
Dreyfus-Brisac C, Larroche JC (1971) Electroencéphalogrammes discontinus du nouveau-né prématuré et à terme. Corrélations électro-anatoma-cliniques (Discontinuous electroencephalograms in the premature newborn and at term. Electro-anatomo-clinical correlations). Rev Electroencephalogr Neurophysiol Clin 1:95–99. https://doi.org/10.1016/s0370-4475(71)80022-9
Duan H, Wearne SL, Rocher AB, Macedo A, Morrison JH, Hof PR (2003) Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb Cortex 13:950–961. https://doi.org/10.1093/cercor/13.9.950
Dunaevsky A, Tashiro A, Majewska A, Mason C, Yuste R (1999) Developmental regulation of spine motility in the mammalian central nervous system. Proc Natl Acad Sci U S A 96:13438–13443. https://doi.org/10.1073/pnas.96.23.13438
Duque A, Krsnik Z, Kostović I, Rakic P (2016) Secondary expansion of the transient subplate zone in the developing cerebrum of human and nonhuman primates. Proc Natl Acad Sci U S A 113:9892–9897. https://doi.org/10.1073/pnas.1610078113
Ehrlich I, Klein M, Rumpel S, Malinow R (2007) PSD-95 is required for activity-driven synapse stabilization. Proc Natl Acad Sci U S A 104:4176–4181. https://doi.org/10.1073/pnas.0609307104
Elias LAB, Kriegstein AR (2008) Gap junctions: multifaceted regulators of embryonic cortical development. Trends Neurosci 31:243–250. https://doi.org/10.1016/j.tins.2008.02.007
Elston GN, Fujita I (2014) Pyramidal cell development: postnatal spinogenesis, dendritic growth, axon growth, and electrophysiology. Front Neuroanat 8:78. https://doi.org/10.3389/fnana.2014.00078
Elston GN, Oga T, Fujita I (2009) Spinogenesis and pruning scales across functional hierarchies. J Neurosci 29:3271–3275. https://doi.org/10.1523/JNEUROSCI.5216-08.2009
Elston GN, Oga T, Okamoto T, Fujita I (2010a) Spinogenesis and pruning from early visual onset to adulthood: an intracellular injection study of layer III pyramidal cells in the ventral visual cortical pathway of the macaque monkey. Cereb Cortex 20:1398–1408. https://doi.org/10.1093/cercor/bhp203
Elston GN, Okamoto T, Oga T, Dornan D, Fujita I (2010b) Spinogenesis and pruning in the primary auditory cortex of the macaque monkey (Macaca fascicularis): an intracellular injection study of layer III pyramidal cells. Brain Res 1316:35–42. https://doi.org/10.1016/j.brainres.2009.12.056
Elston GN, Benavides-Piccione R, Elston A, Manger PR, DeFelipe J (2011a) Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species. Front Neuroanat 5:2. https://doi.org/10.3389/fnana.2011.00002
Elston GN, Oga T, Okamoto T, Fujita I (2011b) Spinogenesis and pruning in the anterior ventral inferotemporal cortex of the macaque monkey: an intracellular injection study of layer III pyramidal cells. Front Neuroanat 5:42. https://doi.org/10.3389/fnana.2011.00042
Engisch KL, Wang X, Rich MM (2022) Homeostatic plasticity of the mammalian neuromuscular junction. Adv Neurobiol 28:111–130. https://doi.org/10.1007/978-3-031-07167-6_5
Enwright Iii JF, Arion D, MacDonald WA, Elbakri R, Pan Y, Vyas G, Berndt A, Lewis DA (2022) Differential gene expression in layer 3 pyramidal neurons across 3 regions of the human cortical visual spatial working memory network. Cereb Cortex 32:5216–5229. https://doi.org/10.1093/cercor/bhac009
Eze UC, Bhaduri A, Haeussler M, Nowakowski TJ, Kriegstein AR (2021) Single-cell atlas of early human brain development highlights heterogeneity of human neuroepithelial cells and early radial glia. Nat Neurosci 24:584–594. https://doi.org/10.1038/s41593-020-00794-1
Fabrizi L, Slater R, Worley A, Meek J, Boyd S, Olhede S, Fitzgerald M (2011) A shift in sensory processing that enables the developing human brain to discriminate touch from pain. Curr Biol 21:1552–1558. https://doi.org/10.1016/j.cub.2011.08.010
Fagard J, Esseily R, Jacquey L, O’Regan K, Somogyi E (2018) Fetal origin of sensorimotor behavior. Front Neurorobot 12:23. https://doi.org/10.3389/fnbot.2018.00023
Faust TE, Gunner G, Schafer DP (2021) Mechanisms governing activity-dependent synaptic pruning in the developing mammalian CNS. Nat Rev Neurosci 22:657–673. https://doi.org/10.1038/s41583-021-00507-y
Finn ES, Huber L, Jangraw DC, Molfese PJ, Bandettini PA (2019) Layer-dependent activity in human prefrontal cortex during working memory. Nat Neurosci 22:1687–1695. https://doi.org/10.1038/s41593-019-0487-z
Fischer M, Kaech S, Knutti D, Matus A (1998) Rapid actin-based plasticity in dendritic spines. Neuron 20:847–854. https://doi.org/10.1016/S0896-6273(00)80467-5
Fish KN, Hoftman GD, Sheikh W, Kitchens M, Lewis DA (2013) Parvalbumin-containing chandelier and basket cell boutons have distinctive modes of maturation in monkey prefrontal cortex. J Neurosci 33:8352–8358. https://doi.org/10.1523/JNEUROSCI.0306-13.2013
Fitzgerald M (2005) The development of nociceptive circuits. Nat Rev Neurosci 6:507–520. https://doi.org/10.1038/nrn1701
Friauf E, McConnell SK, Shatz CJ (1990) Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex. J Neurosci 10:2601–2613. https://doi.org/10.1523/JNEUROSCI.10-08-02601.1990
Frankfurt M, Nassrallah Z, Luine V (2023) Steroid hormone interaction with dendritic spines: implications for neuropsychiatric disease. In: Rasia-Filho AA et al (eds) Dendritic spines. Springer, Cham
Fricker M, Tolkovsky AM, Borutaite V, Coleman M, Brown GC (2018) Neuronal cell death. Physiol Rev 98:813–880. https://doi.org/10.1152/physrev.00011.2017
Friedman NP, Robbins TW (2022) The role of prefrontal cortex in cognitive control and executive function. Neuropsychopharmacology 47:72–89. https://doi.org/10.1038/s41386-021-01132-0
Fritschy JM, Garey LJ (1986) Quantitative changes in morphological parameters in the developing visual cortex of the marmoset monkey. Brain Res 394:173–188. https://doi.org/10.1016/0165-3806(86)90093-3
Fu M, Zuo Y (2011) Experience-dependent structural plasticity in the cortex. Trends Neurosci 34:177–187. https://doi.org/10.1016/j.tins.2011.02.001
Fu M, Yu X, Lu J, Zuo Y (2012) Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo. Nature 483:92–95. https://doi.org/10.1038/nature10844
Fulford J, Vadeyar SH, Dodampahala SH, Moore RJ, Young P, Baker PN, James DK, Gowland PA (2003) Fetal brain activity in response to a visual stimulus. Hum Brain Mapp 20:239–245. https://doi.org/10.1002/hbm.10139
Fuster JM (2008) Anatomy of the prefrontal cortex. In: The prefrontal cortex. Elsevier, Amsterdam, pp 7–58
Galakhova AA, Hunt S, Wilbers R, Heyer DB, de Kock CPJ, Mansvelder HD, Goriounova NA (2022) Evolution of cortical neurons supporting human cognition. Trends Cogn Sci 26:909–922. https://doi.org/10.1016/j.tics.2022.08.012
Gallinaro JV, Gašparović N, Rotter S (2022) Homeostatic control of synaptic rewiring in recurrent networks induces the formation of stable memory engrams. PLoS Comput Biol 18:e1009836. https://doi.org/10.1371/journal.pcbi.1009836
Ganapathee DS, Gunz P (2023) Insights into brain evolution through the genotype-phenotype connection. Prog Brain Res 275:73–92. https://doi.org/10.1016/bs.pbr.2022.12.013
Garcia N, Hernández P, Lanuza MA, Tomàs M, Cilleros-Mañé V, Just-Borràs L, Duran-Vigara M, Polishchuk A, Balanyà-Segura M, Tomàs J (2022) Involvement of the voltage-gated calcium channels L- P/Q- and N-types in synapse elimination during neuromuscular junction development. Mol Neurobiol 59:4044–4064. https://doi.org/10.1007/s12035-022-02818-2
Garcia-Marin V, Ahmed TH, Afzal YC, Hawken MJ (2013) Distribution of vesicular glutamate transporter 2 (VGluT2) in the primary visual cortex of the macaque and human. J Comp Neurol 521:130–151. https://doi.org/10.1002/cne.23165
Garey LJ (1984) Structural development of the visual system of man. Hum Neurobiol 3:75–80
Garey LJ, de Courten C (1983) Structural development of the lateral geniculate nucleus and visual cortex in monkey and man. Behav Brain Res 10:3–13. https://doi.org/10.1016/0166-4328(83)90145-6
Garey LJ, Powell TP (1971) An experimental study of the termination of the lateral geniculo-cortical pathway in the cat and monkey. Proc R Soc Lond B Biol Sci 179:41–63. https://doi.org/10.1098/rspb.1971.0080
Geden MJ, Romero SE, Deshmukh M (2019) Apoptosis versus axon pruning: molecular intersection of two distinct pathways for axon degeneration. Neurosci Res 139:3–8. https://doi.org/10.1016/j.neures.2018.11.007
Ghose P, Shaham S (2020) Cell death in animal development. Development 147. https://doi.org/10.1242/dev.191882
Giannaris EL, Rosene DL (2012) A stereological study of the numbers of neurons and glia in the primary visual cortex across the lifespan of male and female rhesus monkeys. J Comp Neurol 520:3492–3508. https://doi.org/10.1002/cne.23101
Gipson CD, Olive MF (2017) Structural and functional plasticity of dendritic spines – root or result of behavior? Genes Brain Behav 16:101–117. https://doi.org/10.1111/gbb.12324
Glantz LA, Gilmore JH, Hamer RM, Lieberman JA, Jarskog LF (2007) Synaptophysin and postsynaptic density protein 95 in the human prefrontal cortex from mid-gestation into early adulthood. Neuroscience 149:582–591. https://doi.org/10.1016/j.neuroscience.2007.06.036
Glausier JR, Lewis DA (2018) Mapping pathologic circuitry in schizophrenia. Handb Clin Neurol 150:389–417. https://doi.org/10.1016/B978-0-444-63639-3.00025-6
Glucksmann A (1951) Cell deaths in normal vertebrate ontogeny. Biol Rev Camb Philos Soc 26:59–86. https://doi.org/10.1111/j.1469-185x.1951.tb00774.x
Goldman-Rakic PS (1999) The “psychic” neuron of the cerebral cortex. Ann N Y Acad Sci 868:13–26. https://doi.org/10.1111/j.1749-6632.1999.tb11270.x
Goldman-Rakic PS, Brown RM (1982) Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys. Brain Res 256:339–349. https://doi.org/10.1016/0165-3806(82)90146-8
Granger B, Tekaia F, Le Sourd AM, Rakic P, Bourgeois JP (1995) Tempo of neurogenesis and synaptogenesis in the primate cingulate mesocortex: comparison with the neocortex. J Comp Neurol 360:363–376. https://doi.org/10.1002/cne.903600212
Gray EG (1959) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183:1592–1593. https://doi.org/10.1038/1831592a0
Groenewegen HJ, Uylings HB (2000) The prefrontal cortex and the integration of sensory, limbic and autonomic information. Prog Brain Res 126:3–28. https://doi.org/10.1016/S0079-6123(00)26003-2
Groenewegen HJ, Wright CI, Uylings HB (1997) The anatomical relationships of the prefrontal cortex with limbic structures and the basal ganglia. J Psychopharmacol 11:99–106. https://doi.org/10.1177/026988119701100202
Grutzendler J, Kasthuri N, Gan W-B (2002) Long-term dendritic spine stability in the adult cortex. Nature 420:812–816. https://doi.org/10.1038/nature01276
Guardiola-Ripoll M, Fatjó-Vilas M (2023) A systematic review of the human accelerated regions in schizophrenia and related disorders: where the evolutionary and neurodevelopmental hypotheses converge. Int J Mol Sci 24. https://doi.org/10.3390/ijms24043597
Hadders-Algra M (2007) Putative neural substrate of normal and abnormal general movements. Neurosci Biobehav Rev 31:1181–1190. https://doi.org/10.1016/j.neubiorev.2007.04.009
Hadders-Algra M (2018a) Early human brain development: starring the subplate. Neurosci Biobehav Rev 92:276–290. https://doi.org/10.1016/j.neubiorev.2018.06.017
Hadders-Algra M (2018b) Neural substrate and clinical significance of general movements: an update. Dev Med Child Neurol 60:39–46. https://doi.org/10.1111/dmcn.13540
Han DH, Park P, Choi DI, Bliss TVP, Kaang B-K (2022) The essence of the engram: cellular or synaptic? Semin Cell Dev Biol 125:122–135. https://doi.org/10.1016/j.semcdb.2021.05.033
Hansen DV, Lui JH, Parker PRL, Kriegstein AR (2010) Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554–561. https://doi.org/10.1038/nature08845
Harris LW, Lockstone HE, Khaitovich P, Weickert CS, Webster MJ, Bahn S (2009) Gene expression in the prefrontal cortex during adolescence: implications for the onset of schizophrenia. BMC Med Genet 2:28. https://doi.org/10.1186/1755-8794-2-28
Harvey CD, Svoboda K (2007) Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450:1195–1200. https://doi.org/10.1038/nature06416
Hazan L, Ziv NE (2020) Activity dependent and independent determinants of synaptic size diversity. J Neurosci 40:2828–2848. https://doi.org/10.1523/JNEUROSCI.2181-19.2020
He Z, Han D, Efimova O, Guijarro P, Yu Q, Oleksiak A, Jiang S, Anokhin K, Velichkovsky B, Grünewald S, Khaitovich P (2017) Comprehensive transcriptome analysis of neocortical layers in humans, chimpanzees and macaques. Nat Neurosci 20:886–895. https://doi.org/10.1038/nn.4548
He LX, Wan L, Xiang W, Li JM, Pan AH, Lu DH (2020) Synaptic development of layer V pyramidal neurons in the prenatal human prefrontal neocortex: a Neurolucida-aided Golgi study. Neural Regen Res 15:1490–1495. https://doi.org/10.4103/1673-5374.274345
Hebb DO (1949) The organization of behavior; a neuropsychological theory. The organization of behavior, a neuropsychological theory. Wiley, Oxford
Heck N, Santos MD (2023) Dendritic spines in learning and memory: from first discoveries to current insights. In: Rasia-Filho AA et al (eds) Dendritic spines. Springer, Cham
Heckman EL, Doe CQ (2021) Establishment and maintenance of neural circuit architecture. J Neurosci 41:1119–1129. https://doi.org/10.1523/JNEUROSCI.1143-20.2020
Herrmann K, Shatz CJ (1995) Blockade of action potential activity alters initial arborization of thalamic axons within cortical layer 4. Proc Natl Acad Sci U S A 92:11244–11248. https://doi.org/10.1073/pnas.92.24.11244
Herrmann K, Antonini A, Shatz CJ (1994) Ultrastructural evidence for synaptic interactions between thalamocortical axons and subplate neurons. Eur J Neurosci 6:1729–1742. https://doi.org/10.1111/j.1460-9568.1994.tb00565.x
Hevner RF (2000) Development of connections in the human visual system during fetal mid-gestation: a DiI-tracing study. J Neuropathol Exp Neurol 59:385–392. https://doi.org/10.1093/jnen/59.5.385
Ho VM, Lee JA, Martin KC (2011) The cell biology of synaptic plasticity. Science 334:623–628. https://doi.org/10.1126/science.1209236
Hodel AS (2018) Rapid infant prefrontal cortex development and sensitivity to early environmental experience. Dev Rev 48:113–144. https://doi.org/10.1016/j.dr.2018.02.003
Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hübener M (2009) Experience leaves a lasting structural trace in cortical circuits. Nature 457:313–317. https://doi.org/10.1038/nature07487
Hoftman GD, Datta D, Lewis DA (2017) Layer 3 excitatory and inhibitory circuitry in the prefrontal cortex: developmental trajectories and alterations in schizophrenia. Biol Psychiatry 81:862–873. https://doi.org/10.1016/j.biopsych.2016.05.022
Hoftman GD, Bazmi HH, Ciesielski AJ, Dinka LA, Chen K, Lewis DA (2021) Postnatal development of glutamate and GABA transcript expression in monkey visual, parietal, and prefrontal cortices. Cereb Cortex 31:2026–2037. https://doi.org/10.1093/cercor/bhaa342
Holtmaat A, Caroni P (2016) Functional and structural underpinnings of neuronal assembly formation in learning. Nat Neurosci 19:1553–1562. https://doi.org/10.1038/nn.4418
Holtmaat AJGD, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45:279–291. https://doi.org/10.1016/j.neuron.2005.01.003
Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K (2006) Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 441:979–983. https://doi.org/10.1038/nature04783
Honkura N, Matsuzaki M, Noguchi J, Ellis-Davies GC, Kasai H (2008) The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 57:719–729. https://doi.org/10.1016/j.neuron.2008.01.013
Horrell ND, Acosta MC, Saltzman W (2021) Plasticity of the paternal brain: effects of fatherhood on neural structure and function. Dev Psychobiol 63:1499–1520. https://doi.org/10.1002/dev.22097
Hrabač P, Bosak A, Vukšić M, Judaš M, Kostović I, Krsnik Ž (2018) The Zagreb collection of human brains: entering the virtual world. Croat Med J 59:283–287. https://doi.org/10.3325/10.3325/cmj.2018.59.283
Hrvoj-Mihic B, Semendeferi K (2019) Neurodevelopmental disorders of the prefrontal cortex in an evolutionary context. Prog Brain Res 250:109–127. https://doi.org/10.1016/bs.pbr.2019.05.003
Huang Z, Wang Q, Zhou S, Tang C, Yi F, Nie J (2020) Exploring functional brain activity in neonates: a resting-state fMRI study. Dev Cogn Neurosci 45:100850. https://doi.org/10.1016/j.dcn.2020.100850
Hubel DH, Wiesel TN (1963) Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J Neurophysiol 26:994–1002. https://doi.org/10.1152/jn.1963.26.6.994
Hubel DH, Wiesel TN (1965) Binocular interaction in striate cortex of kittens reared with artificial squint. J Neurophysiol 28:1041–1059. https://doi.org/10.1152/jn.1965.28.6.1041
Hubel DH, Wiesel TN (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol 206:419–436. https://doi.org/10.1113/jphysiol.1970.sp009022
Hubel DH, Wiesel TN, LeVay S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond Ser B Biol Sci 278:377–409. https://doi.org/10.1098/rstb.1977.0050
Huberman AD, Speer CM, Chapman B (2006) Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in v1. Neuron 52:247–254. https://doi.org/10.1016/j.neuron.2006.07.028
Hublin J-J, Changeux J-P (2022) Paleoanthropology of cognition: an overview on hominins brain evolution. C R Biol 345:57–75. https://doi.org/10.5802/crbiol.92
Hunnicutt BJ, Krzywinski M (2016) Neural circuit diagrams. Nat Methods 13:189. https://doi.org/10.1038/nmeth.3777
Hunt S, Leibner Y, Mertens EJ, Barros-Zulaica N, Kanari L, Heistek TS, Karnani MM, Aardse R, Wilbers R, Heyer DB, Goriounova NA, Verhoog MB, Testa-Silva G, Obermayer J, Versluis T, Benavides-Piccione R, de Witt-Hamer P, Idema S, Noske DP, Baayen JC, Lein ES, DeFelipe J, Markram H, Mansvelder HD, Schürmann F, Segev I, de Kock CPJ (2023) Strong and reliable synaptic communication between pyramidal neurons in adult human cerebral cortex. Cereb Cortex 33:2857–2878. https://doi.org/10.1093/cercor/bhac246
Huttenlocher PR (1979) Synaptic density in human frontal cortex – developmental changes and effects of aging. Brain Res 163:195–205. https://doi.org/10.1016/0006-8993(79)90349-4
Huttenlocher PR, Dabholkar AS (1997) Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387:167–178. https://doi.org/10.1002/(SICI)1096-9861(19971020)387:2<167:AID-CNE1>3.0.CO;2-Z
Huttenlocher PR, de Courten C (1987) The development of synapses in striate cortex of man. Hum Neurobiol 6:1–9
Huttenlocher PR, de Courten C, Garey LJ, van der Loos H (1982) Synaptogenesis in human visual cortex--evidence for synapse elimination during normal development. Neurosci Lett 33:247–252. https://doi.org/10.1016/0304-3940(82)90379-2
Huuki-Myers L, Spangler A, Eagles N, Montgomery KD, Kwon SH, Guo B, Grant-Peters M, Divecha HR, Tippani M, Sriworarat C, Nguyen AB, Ravichandran P, Tran MN, Seyedian A, Hyde TM, Kleinman JE, Battle A, Page SC, Ryten M, Hicks SC, Martinowich K, Collado-Torres L, Maynard KR (2023) Integrated single cell and unsupervised spatial transcriptomic analysis defines molecular anatomy of the human dorsolateral prefrontal cortex. bioRxiv. https://doi.org/10.1101/2023.02.15.528722
Innocenti GM (1981) Growth and reshaping of axons in the establishment of visual callosal connections. Science 212:824–827. https://doi.org/10.1126/science.7221566
Innocenti GM, Price DJ (2005) Exuberance in the development of cortical networks. Nat Rev Neurosci 6:955–965. https://doi.org/10.1038/nrn1790
Innocenti GM, Schmidt K, Milleret C, Fabri M, Knyazeva MG, Battaglia-Mayer A, Aboitiz F, Ptito M, Caleo M, Marzi CA, Barakovic M, Lepore F, Caminiti R (2022) The functional characterization of callosal connections. Prog Neurobiol 208:102186. https://doi.org/10.1016/j.pneurobio.2021.102186
Islam KUS, Meli N, Blaess S (2021) The development of the mesoprefrontal dopaminergic system in health and disease. Front Neural Circuits 15:746582. https://doi.org/10.3389/fncir.2021.746582
Jacobs B, Scheibel AB (1993) A quantitative dendritic analysis of Wernicke’s area in humans. I. Lifespan changes. J Comp Neurol 327:83–96. https://doi.org/10.1002/cne.903270107
Jacobs B, Chugani HT, Allada V, Chen S, Phelps ME, Pollack DB, Raleigh MJ (1995) Developmental changes in brain metabolism in sedated rhesus macaques and vervet monkeys revealed by positron emission tomography. Cereb Cortex 5:222–233. https://doi.org/10.1093/cercor/5.3.222
Jacobs B, Driscoll L, Schall M (1997) Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J Comp Neurol 386:661–680. https://doi.org/10.1002/(SICI)1096-9861(19971006)386:4<661:AID-CNE11>3.0.CO;2-N
Jardri R, Pins D, Houfflin-Debarge V, Chaffiotte C, Rocourt N, Pruvo J-P, Steinling M, Delion P, Thomas P (2008) Fetal cortical activation to sound at 33 weeks of gestation: a functional MRI study. NeuroImage 42:10–18. https://doi.org/10.1016/j.neuroimage.2008.04.247
Jenks KR, Tsimring K, Ip JPK, Zepeda JC, Sur M (2021) Heterosynaptic plasticity and the experience-dependent refinement of developing neuronal circuits. Front Neural Circuits 15:803401. https://doi.org/10.3389/fncir.2021.803401
Jensen KT, Kadmon Harpaz N, Dhawale AK, Wolff SBE, Ölveczky BP (2022) Long-term stability of single neuron activity in the motor system. Nat Neurosci 25:1664–1674. https://doi.org/10.1038/s41593-022-01194-3
Ji L, Majbri A, Hendrix CL, Thomason ME (2023) Fetal behavior during MRI changes with age and relates to network dynamics. Hum Brain Mapp 44:1683–1694. https://doi.org/10.1002/hbm.26167
Josselyn SA, Tonegawa S (2020) Memory engrams: recalling the past and imagining the future. Science 367. https://doi.org/10.1126/science.aaw4325
Judaš M, Šimić G, Petanjek Z, Jovanov-Milošević N, Pletikos M, Vasung L, Vukšić M, Kostović I (2011) The Zagreb collection of human brains: a unique, versatile, but underexploited resource for the neuroscience community. Ann N Y Acad Sci 1225(Suppl 1):E105–E130. https://doi.org/10.1111/j.1749-6632.2011.05993.x
Kanazawa H, Yamada Y, Tanaka K, Kawai M, Niwa F, Iwanaga K, Kuniyoshi Y (2023) Open-ended movements structure sensorimotor information in early human development. Proc Natl Acad Sci U S A 120:e2209953120. https://doi.org/10.1073/pnas.2209953120
Kanjhan R, Fogarty MJ, Noakes PG, Bellingham MC (2016) Developmental changes in the morphology of mouse hypoglossal motor neurons. Brain Struct Funct 221:3755–3786. https://doi.org/10.1007/s00429-015-1130-8
Kasai H, Hayama T, Ishikawa M, Watanabe S, Yagishita S, Noguchi J (2010) Learning rules and persistence of dendritic spines. Eur J Neurosci 32:241–249. https://doi.org/10.1111/j.1460-9568.2010.07344.x
Kasai H, Ziv NE, Okazaki H, Yagishita S, Toyoizumi T (2021) Spine dynamics in the brain, mental disorders and artificial neural networks. Nat Rev Neurosci 22:407–422. https://doi.org/10.1038/s41583-021-00467-3
Katušić A, Žunić Išasegi I, Radoš M, Raguž M, Grizelj R, Ferrari F, Kostović I (2021) Transient structural MRI patterns correlate with the motor functions in preterm infants. Brain and Development 43:363–371. https://doi.org/10.1016/j.braindev.2020.11.002
Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133–1138. https://doi.org/10.1126/science.274.5290.1133
Keck T, Mrsic-Flogel TD, Vaz Afonso M, Eysel UT, Bonhoeffer T, Hübener M (2008) Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nat Neurosci 11:1162–1167. https://doi.org/10.1038/nn.2181
Keller-Peck CR, Walsh MK, Gan WB, Feng G, Sanes JR, Lichtman JW (2001) Asynchronous synapse elimination in neonatal motor units: studies using GFP transgenic mice. Neuron 31:381–394. https://doi.org/10.1016/s0896-6273(01)00383-x
Khazipov R, Esclapez M, Caillard O, Bernard C, Khalilov I, Tyzio R, Hirsch J, Dzhala V, Berger B, Ben-Ari Y (2001) Early development of neuronal activity in the primate hippocampus in utero. J Neurosci 21:9770–9781. https://doi.org/10.1523/JNEUROSCI.21-24-09770.2001
Kirchner JH, Gjorgjieva J (2021) Emergence of local and global synaptic organization on cortical dendrites. Nat Commun 12:4005. https://doi.org/10.1038/s41467-021-23557-3
Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K (2006) Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci 9:1117–1124. https://doi.org/10.1038/nn1747
Koehler RC (2021) Regulation of the cerebral circulation during development. Compr Physiol 11:2371–2432. https://doi.org/10.1002/cphy.c200028
Koenderink MJ, Uylings HB (1995) Postnatal maturation of layer V pyramidal neurons in the human prefrontal cortex. A quantitative Golgi analysis. Brain Res 678:233–243. https://doi.org/10.1016/0006-8993(95)00206-6
Koenderink MJ, Uylings HB, Mrzljak L (1994) Postnatal maturation of the layer III pyramidal neurons in the human prefrontal cortex: a quantitative Golgi analysis. Brain Res 653:173–182. https://doi.org/10.1016/0006-8993(94)90387-5
Koester SE, O’Leary DD (1992) Functional classes of cortical projection neurons develop dendritic distinctions by class-specific sculpting of an early common pattern. J Neurosci 12:1382–1393. https://doi.org/10.1523/JNEUROSCI.12-04-01382.1992
Kolb B, Mychasiuk R, Muhammad A, Li Y, Frost DO, Gibb R (2012) Experience and the developing prefrontal cortex. Proc Natl Acad Sci U S A 109(Suppl 2):17186–17193. https://doi.org/10.1073/pnas.1121251109
Kopić J, Junaković A, Salamon I, Rasin M-R, Kostović I, Krsnik Ž (2023) Early regional patterning in the human prefrontal cortex revealed by laminar dynamics of deep projection neuron markers. Cell 12. https://doi.org/10.3390/cells12020231
Korponay C, Choi EY, Haber SN (2020) Corticostriatal projections of macaque area 44. Cereb Cortex Commun 1:tgaa079. https://doi.org/10.1093/texcom/tgaa079
Kostović I (1986) Prenatal development of nucleus basalis complex and related fiber systems in man: a histochemical study. Neuroscience 17:1047–1077. https://doi.org/10.1016/0306-4522(86)90077-1
Kostović I (2020) The enigmatic fetal subplate compartment forms an early tangential cortical nexus and provides the framework for construction of cortical connectivity. Prog Neurobiol 194:101883. https://doi.org/10.1016/j.pneurobio.2020.101883
Kostovic I, Goldman-Rakic PS (1983) Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain. J Comp Neurol 219:431–447. https://doi.org/10.1002/cne.902190405
Kostović I, Jovanov-Milosević N (2006) The development of cerebral connections during the first 20–45 weeks’ gestation. Semin Fetal Neonatal Med 11:415–422. https://doi.org/10.1016/j.siny.2006.07.001
Kostović I, Judas M (2002) Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anat Rec 267:1–6. https://doi.org/10.1002/ar.10069
Kostovic I, Judas M (2006) Prolonged coexistence of transient and permanent circuitry elements in the developing cerebral cortex of fetuses and preterm infants. Dev Med Child Neurol 48:388–393. https://doi.org/10.1017/S0012162206000831
Kostović I, Judas M (2010) The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatr 99:1119–1127. https://doi.org/10.1111/j.1651-2227.2010.01811.x
Kostović I, Judaš M (2015) Embryonic and fetal development of the human cerebral cortex. In: Brain mapping. Elsevier, Amsterdam, pp 167–175
Kostovic I, Rakic P (1980) Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. J Neurocytol 9:219–242. https://doi.org/10.1007/BF01205159
Kostovic I, Rakic P (1984) Development of prestriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesterase staining. J Neurosci 4:25–42. https://doi.org/10.1523/JNEUROSCI.04-01-00025.1984
Kostovic I, Rakic P (1990) Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297:441–470. https://doi.org/10.1002/cne.902970309
Kostović I, Jovanov-Milošević N, Radoš M, Sedmak G, Benjak V, Kostović-Srzentić M, Vasung L, Čuljat M, Radoš M, Hüppi P, Judaš M (2014) Perinatal and early postnatal reorganization of the subplate and related cellular compartments in the human cerebral wall as revealed by histological and MRI approaches. Brain Struct Funct 219:231–253. https://doi.org/10.1007/s00429-012-0496-0
Kostović I, Radoš M, Kostović-Srzentić M, Krsnik Ž (2021) Fundamentals of the development of connectivity in the human fetal brain in late gestation: from 24 weeks gestational age to term. J Neuropathol Exp Neurol 80:393–414. https://doi.org/10.1093/jnen/nlab024
Kourosh-Arami M, Hosseini N, Komaki A (2021) Brain is modulated by neuronal plasticity during postnatal development. J Physiol Sci 71:34. https://doi.org/10.1186/s12576-021-00819-9
Kozorovitskiy Y, Hughes M, Lee K, Gould E (2006) Fatherhood affects dendritic spines and vasopressin V1a receptors in the primate prefrontal cortex. Nat Neurosci 9:1094–1095. https://doi.org/10.1038/nn1753
Kristiansen M, Ham J (2014) Programmed cell death during neuronal development: the sympathetic neuron model. Cell Death Differ 21:1025–1035. https://doi.org/10.1038/cdd.2014.47
Krmpotić-Nemanić J, Kostović I, Kelović Z, Nemanić D, Mrzljak L (1983) Development of the human fetal auditory cortex: growth of afferent fibres. Acta Anat (Basel) 116:69–73
Kroeze Y, Oti M, van Beusekom E, Cooijmans RHM, van Bokhoven H, Kolk SM, Homberg JR, Zhou H (2018) Transcriptome analysis identifies multifaceted regulatory mechanisms dictating a genetic switch from neuronal network establishment to maintenance during postnatal prefrontal cortex development. Cereb Cortex 28:833–851. https://doi.org/10.1093/cercor/bhw407
Krsnik Ž, Majić V, Vasung L, Huang H, Kostović I (2017) Growth of thalamocortical fibers to the somatosensory cortex in the human fetal brain. Front Neurosci 11:233. https://doi.org/10.3389/fnins.2017.00233
Kruijssen DLH, Wierenga CJ (2019) Single synapse LTP: a matter of context? Front Cell Neurosci 13:496. https://doi.org/10.3389/fncel.2019.00496
Kugelberg E (1976) Adaptive transformation of rat soleus motor units during growth. J Neurol Sci 27:269–289. https://doi.org/10.1016/0022-510x(76)90001-0
Lagercrantz H, Changeux J-P (2010) Basic consciousness of the newborn. Semin Perinatol 34:201–206. https://doi.org/10.1053/j.semperi.2010.02.004
Lamantia AS, Rakic P (1990a) Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey. J Neurosci 10:2156–2175. https://doi.org/10.1523/JNEUROSCI.10-07-02156.1990
Lamantia AS, Rakic P (1990b) Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey. J Comp Neurol 291:520–537. https://doi.org/10.1002/cne.902910404
Lamantia AS, Rakic P (1994) Axon overproduction and elimination in the anterior commissure of the developing rhesus monkey. J Comp Neurol 340:328–336. https://doi.org/10.1002/cne.903400304
Lamprecht R, LeDoux J (2004) Structural plasticity and memory. Nat Rev Neurosci 5:45–54. https://doi.org/10.1038/nrn1301
Larsen B, Luna B (2018) Adolescence as a neurobiological critical period for the development of higher-order cognition. Neurosci Biobehav Rev 94:179–195. https://doi.org/10.1016/j.neubiorev.2018.09.005
Lee YI (2020) Developmental neuromuscular synapse elimination: activity-dependence and potential downstream effector mechanisms. Neurosci Lett 718:134724. https://doi.org/10.1016/j.neulet.2019.134724
Lee W, Donner EJ, Nossin-Manor R, Whyte HEA, Sled JG, Taylor MJ (2012) Visual functional magnetic resonance imaging of preterm infants. Dev Med Child Neurol 54:724–729. https://doi.org/10.1111/j.1469-8749.2012.04342.x
Lee JH, Kim WB, Park EH, Cho JH (2023) Neocortical synaptic engrams for remote contextual memories. Nat Neurosci 26:259–273. https://doi.org/10.1038/s41593-022-01223-1
Leisman G (2022) On the application of developmental cognitive neuroscience in educational environments. Brain Sci 12. https://doi.org/10.3390/brainsci12111501
Leuba G, Kraftsik R (1994) Changes in volume, surface estimate, three-dimensional shape and total number of neurons of the human primary visual cortex from midgestation until old age. Anat Embryol (Berl) 190:351–366. https://doi.org/10.1007/BF00187293
Lichtman JW (1977) The reorganization of synaptic connexions in the rat submandibular ganglion during post-natal development. J Physiol 273:155–177. https://doi.org/10.1113/jphysiol.1977.sp012087
Lichtman JW, Colman H (2000) Synapse elimination and indelible memory. Neuron 25:269–278. https://doi.org/10.1016/S0896-6273(00)80893-4
Lidow MS, Rakic P (1992) Scheduling of monoaminergic neurotransmitter receptor expression in the primate neocortex during postnatal development. Cereb Cortex 2:401–416. https://doi.org/10.1093/cercor/2.5.401
Lidow MS, Goldman-Rakic PS, Rakic P (1991) Synchronized overproduction of neurotransmitter receptors in diverse regions of the primate cerebral cortex. Proc Natl Acad Sci U S A 88:10218–10221. https://doi.org/10.1073/pnas.88.22.10218
Lin W, Dominguez B, Yang J, Aryal P, Brandon EP, Gage FH, Lee KF (2005) Neurotransmitter acetylcholine negatively regulates neuromuscular synapse formation by a Cdk5-dependent mechanism. Neuron 46:569–579. https://doi.org/10.1016/j.neuron.2005.04.002
Liu X, Somel M, Tang L, Yan Z, Jiang X, Guo S, Yuan Y, He L, Oleksiak A, Zhang Y, Li N, Hu Y, Chen W, Qiu Z, Pääbo S, Khaitovich P (2012) Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques. Genome Res 22:611–622. https://doi.org/10.1101/gr.127324.111
Lohof AM, Delhaye-Bouchaud N, Mariani J (1996) Synapse elimination in the central nervous system: functional significance and cellular mechanisms. Rev Neurosci 7:85–101. https://doi.org/10.1515/revneuro.1996.7.2.85
Lomo T (1968) Potentiation of monosynaptic EPSPs in cortical cells by single and repetitive afferent volleys. J Physiol 194:84–5P
Lømo T (2018) Discovering long-term potentiation (LTP) – recollections and reflections on what came after. Acta Physiol (Oxf) 222. https://doi.org/10.1111/apha.12921
Lübke J, Albus K (1989) The postnatal development of layer VI pyramidal neurons in the cat’s striate cortex, as visualized by intracellular Lucifer yellow injections in aldehyde-fixed tissue. Brain Res Dev Brain Res 45:29–38. https://doi.org/10.1016/0165-3806(89)90004-7
Luengo-Sanchez S, Fernaud-Espinosa I, Bielza C, Benavides-Piccione R, Larrañaga P, DeFelipe J (2018) 3D morphology-based clustering and simulation of human pyramidal cell dendritic spines. PLoS Comput Biol 14:e1006221. https://doi.org/10.1371/journal.pcbi.1006221
Luhmann HJ, Khazipov R (2018) Neuronal activity patterns in the developing barrel cortex. Neuroscience 368:256–267. https://doi.org/10.1016/j.neuroscience.2017.05.025
Luhmann HJ, Kirischuk S, Kilb W (2018) The superior function of the subplate in early neocortical development. Front Neuroanat 12:97. https://doi.org/10.3389/fnana.2018.00097
Luhmann HJ, Kanold PO, Molnár Z, Vanhatalo S (2022) Early brain activity: translations between bedside and laboratory. Prog Neurobiol 213:102268. https://doi.org/10.1016/j.pneurobio.2022.102268
Lund JS, Holbach SM (1991) Postnatal development of thalamic recipient neurons in the monkey striate cortex: I. Comparison of spine acquisition and dendritic growth of layer 4C alpha and beta spiny stellate neurons. J Comp Neurol 309:115–128. https://doi.org/10.1002/cne.903090108
Lund JS, Boothe RG, Lund RD (1977) Development of neurons in the visual cortex (area 17) of the monkey (Macaca nemestrina): a Golgi study from fetal day 127 to postnatal maturity. J Comp Neurol 176:149–188. https://doi.org/10.1002/cne.901760203
Lund JS, Holbach SM, Chung WW (1991) Postnatal development of thalamic recipient neurons in the monkey striate cortex: II. Influence of afferent driving on spine acquisition and dendritic growth of layer 4C spiny stellate neurons. J Comp Neurol 309:129–140. https://doi.org/10.1002/cne.903090109
Luo L, O’Leary DDM (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127–156. https://doi.org/10.1146/annurev.neuro.28.061604.135632
Ma S, Zuo Y (2022) Synaptic modifications in learning and memory – a dendritic spine story. Semin Cell Dev Biol 125:84–90. https://doi.org/10.1016/j.semcdb.2021.05.015
Ma S, Skarica M, Li Q, Xu C, Risgaard RD, Tebbenkamp ATN, Mato-Blanco X, Kovner R, Krsnik Ž, de Martin X, Luria V, Martí-Pérez X, Liang D, Karger A, Schmidt DK, Gomez-Sanchez Z, Qi C, Gobeske KT, Pochareddy S, Debnath A, Hottman CJ, Spurrier J, Teo L, Boghdadi AG, Homman-Ludiye J, Ely JJ, Daadi EW, Mi D, Daadi M, Marín O, Hof PR, Rasin M-R, Bourne J, Sherwood CC, Santpere G, Girgenti MJ, Strittmatter SM, Sousa AMM, Sestan N (2022) Molecular and cellular evolution of the primate dorsolateral prefrontal cortex. Science 377:eabo7257. https://doi.org/10.1126/science.abo7257
Magee JC, Grienberger C (2020) Synaptic plasticity forms and functions. Annu Rev Neurosci 43:95–117. https://doi.org/10.1146/annurev-neuro-090919-022842
Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5–21. https://doi.org/10.1016/j.neuron.2004.09.012
Marafiga JR, Calcagnotto ME (2023) Electrophysiology of dendritic spines: information processing, dynamic compartmentalization, and synaptic plasticity. In: Rasia-Filho AA et al (eds) Dendritic spines. Springer, Cham
Marchetto MC, Hrvoj-Mihic B, Kerman BE, Yu DX, Vadodaria KC, Linker SB, Narvaiza I, Santos R, Denli AM, Mendes AP, Oefner R, Cook J, McHenry L, Grasmick JM, Heard K, Fredlender C, Randolph-Moore L, Kshirsagar R, Xenitopoulos R, Chou G, Hah N, Muotri AR, Padmanabhan K, Semendeferi K, Gage FH (2019) Species-specific maturation profiles of human, chimpanzee and bonobo neural cells. Elife 8. https://doi.org/10.7554/eLife.37527
Markus EJ, Petit TL (1987) Neocortical synaptogenesis, aging, and behavior: lifespan development in the motor-sensory system of the rat. Exp Neurol 96:262–278. https://doi.org/10.1016/0014-4886(87)90045-8
Martini FJ, Guillamón-Vivancos T, Moreno-Juan V, Valdeolmillos M, López-Bendito G (2021) Spontaneous activity in developing thalamic and cortical sensory networks. Neuron 109:2519–2534. https://doi.org/10.1016/j.neuron.2021.06.026
Mashour GA, Roelfsema P, Changeux J-P, Dehaene S (2020) Conscious processing and the global neuronal workspace hypothesis. Neuron 105:776–798. https://doi.org/10.1016/j.neuron.2020.01.026
Mates SL, Lund JS (1983) Neuronal composition and development in lamina 4C of monkey striate cortex. J Comp Neurol 221:60–90. https://doi.org/10.1002/cne.902210106
Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761–766. https://doi.org/10.1038/nature02617
Maynard KR, Collado-Torres L, Weber LM, Uytingco C, Barry BK, Williams SR, Catallini JL, Tran MN, Besich Z, Tippani M, Chew J, Yin Y, Kleinman JE, Hyde TM, Rao N, Hicks SC, Martinowich K, Jaffe AE (2021) Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex. Nat Neurosci 24:425–436. https://doi.org/10.1038/s41593-020-00787-0
Mayseless O, Shapira G, Rachad EY, Fiala A, Schuldiner O (2023) Neuronal excitability as a regulator of circuit remodeling. Curr Biol 33:981–989.e3. https://doi.org/10.1016/j.cub.2023.01.032
McAllister AK (2000) Cellular and molecular mechanisms of dendrite growth. Cereb Cortex 10:963–973. https://doi.org/10.1093/cercor/10.10.963
McGuire PK, Bates JF, Goldman-Rakic PS (1991) Interhemispheric integration: II. Symmetry and convergence of the corticostriatal projections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) of the rhesus monkey. Cereb Cortex 1:408–417. https://doi.org/10.1093/cercor/1.5.408
Mencía S, Alonso C, Pallás-Alonso C, López-Herce J, Maternal ACHADNS, II (2022) Evaluation and treatment of pain in fetuses, neonates and children. Children (Basel) 9. https://doi.org/10.3390/children9111688
Meyer G, González-Gómez M (2018) The heterogeneity of human Cajal-Retzius neurons. Semin Cell Dev Biol 76:101–111. https://doi.org/10.1016/j.semcdb.2017.08.059
Meyer G, González-Hernández TH, Ferres-Torres R (1989) The spiny stellate neurons in layer IV of the human auditory cortex. A Golgi study. Neuroscience 33:489–498. https://doi.org/10.1016/0306-4522(89)90401-6
Meyer G, Schaaps JP, Moreau L, Goffinet AM (2000) Embryonic and early fetal development of the human neocortex. J Neurosci 20:1858–1868. https://doi.org/10.1523/JNEUROSCI.20-05-01858.2000
Meyer D, Bonhoeffer T, Scheuss V (2014) Balance and stability of synaptic structures during synaptic plasticity. Neuron 82:430–443. https://doi.org/10.1016/j.neuron.2014.02.031
Michel AE, Garey LJ (1984) The development of dendritic spines in the human visual cortex. Hum Neurobiol 3:223–227
Midorikawa M, Miyata M (2021) Distinct functional developments of surviving and eliminated presynaptic terminals. Proc Natl Acad Sci U S A 118. https://doi.org/10.1073/pnas.2022423118
Milh M, Kaminska A, Huon C, Lapillonne A, Ben-Ari Y, Khazipov R (2007) Rapid cortical oscillations and early motor activity in premature human neonate. Cereb Cortex 17:1582–1594. https://doi.org/10.1093/cercor/bhl069
Miškić T, Kostović I, Rašin M-R, Krsnik Ž (2021) Adult upper cortical layer specific transcription factor CUX2 is expressed in transient subplate and marginal zone neurons of the developing human brain. Cells 10. https://doi.org/10.3390/cells10020415
Missler M, Wolff A, Merker HJ, Wolff JR (1993) Pre- and postnatal development of the primary visual cortex of the common marmoset. II. Formation, remodelling, and elimination of synapses as overlapping processes. J Comp Neurol 333:53–67. https://doi.org/10.1002/cne.903330105
Miyashita Y (2022) Operating principles of the cerebral cortex as a six-layered network in primates: beyond the classic canonical circuit model. Proc Jpn Acad Ser B Phys Biol Sci 98:93–111. https://doi.org/10.2183/pjab.98.007
Molliver ME, Kostović I, van der Loos H (1973) The development of synapses in cerebral cortex of the human fetus. Brain Res 50:403–407. https://doi.org/10.1016/0006-8993(73)90741-5
Molnár Z, Luhmann HJ, Kanold PO (2020) Transient cortical circuits match spontaneous and sensory-driven activity during development. Science 370. https://doi.org/10.1126/science.abb2153
Moore AH, Hovda DA, Cherry SR, Villablanca JP, Pollack DB, Phelps ME (2000) Dynamic changes in cerebral glucose metabolism in conscious infant monkeys during the first year of life as measured by positron emission tomography. Brain Res Dev Brain Res 120:141–150. https://doi.org/10.1016/s0165-3806(00)00005-5
Moore AR, Filipovic R, Mo Z, Rasband MN, Zecevic N, Antic SD (2009) Electrical excitability of early neurons in the human cerebral cortex during the second trimester of gestation. Cereb Cortex 19:1795–1805. https://doi.org/10.1093/cercor/bhn206
Moore AR, Zhou W-L, Jakovcevski I, Zecevic N, Antic SD (2011) Spontaneous electrical activity in the human fetal cortex in vitro. J Neurosci 31:2391–2398. https://doi.org/10.1523/JNEUROSCI.3886-10.2011
Moore AR, Zhou W-L, Sirois CL, Belinsky GS, Zecevic N, Antic SD (2014) Connexin hemichannels contribute to spontaneous electrical activity in the human fetal cortex. Proc Natl Acad Sci U S A 111:E3919–E3928. https://doi.org/10.1073/pnas.1405253111
Moron H, Gagnard-Landra C, Guiraud D, Dupeyron A (2021) Contribution of single-fiber evaluation on monitoring outcomes following injection of botulinum toxin-A: a narrative review of the literature. Toxins (Basel) 13. https://doi.org/10.3390/toxins13050356
Mrzljak L, Uylings HB, Kostovic I, van Eden CG (1988) Prenatal development of neurons in the human prefrontal cortex: I. A qualitative Golgi study. J Comp Neurol 271:355–386. https://doi.org/10.1002/cne.902710306
Mrzljak L, Uylings HB, van Eden CG, Judás M (1990) Neuronal development in human prefrontal cortex in prenatal and postnatal stages. Prog Brain Res 85:185–222. https://doi.org/10.1016/s0079-6123(08)62681-3
Mrzljak L, Uylings HB, Kostovic I, van Eden CG (1992) Prenatal development of neurons in the human prefrontal cortex. II. A quantitative Golgi study. J Comp Neurol 316:485–496. https://doi.org/10.1002/cne.903160408
Mukherjee D, Kanold PO (2022) Changing subplate circuits: early activity dependent circuit plasticity. Front Cell Neurosci 16:1067365. https://doi.org/10.3389/fncel.2022.1067365
Muthukrishna M, Doebeli M, Chudek M, Henrich J (2018) The cultural brain hypothesis: how culture drives brain expansion, sociality, and life history. PLoS Comput Biol 14:e1006504. https://doi.org/10.1371/journal.pcbi.1006504
Muzik O, Janisse J, Ager J, Shen C, Chugani DC, Chugani HT (1999) A mathematical model for the analysis of cross-sectional brain glucose metabolism data in children. Prog Neuro-Psychopharmacol Biol Psychiatry 23:589–600. https://doi.org/10.1016/s0278-5846(99)00018-4
Nagamori A, Laine CM, Loeb GE, Valero-Cuevas FJ (2021) Force variability is mostly not motor noise: theoretical implications for motor control. PLoS Comput Biol 17:e1008707. https://doi.org/10.1371/journal.pcbi.1008707
Nagy C, Maitra M, Tanti A, Suderman M, Théroux J-F, Davoli MA, Perlman K, Yerko V, Wang YC, Tripathy SJ, Pavlidis P, Mechawar N, Ragoussis J, Turecki G (2020) Single-nucleus transcriptomics of the prefrontal cortex in major depressive disorder implicates oligodendrocyte precursor cells and excitatory neurons. Nat Neurosci 23:771–781. https://doi.org/10.1038/s41593-020-0621-y
Nazareth L, St John J, Murtaza M, Ekberg J (2021) Phagocytosis by peripheral glia: importance for nervous system functions and implications in injury and disease. Front Cell Dev Biol 9:660259. https://doi.org/10.3389/fcell.2021.660259
Nelson CA (1994) Threats to optimal development: integrating biological, psychological, and social risk factors. Minnesota symposia on child psychology, vol 27. L. Erlbaum Associates, Hillsdale
Neumane S, Gondova A, Leprince Y, Hertz-Pannier L, Arichi T, Dubois J (2022) Early structural connectivity within the sensorimotor network: deviations related to prematurity and association to neurodevelopmental outcome. Front Neurosci 16:932386. https://doi.org/10.3389/fnins.2022.932386
Nguyen QT, Lichtman JW (1996) Mechanism of synapse disassembly at the developing neuromuscular junction. Curr Opin Neurobiol 6:104–112. https://doi.org/10.1016/s0959-4388(96)80015-8
Nicoll RA (2017) A brief history of long-term potentiation. Neuron 93:281–290. https://doi.org/10.1016/j.neuron.2016.12.015
Nobin A, Björklund A (1973) Topography of the monoamine neuron systems in the human brain as revealed in fetuses. Acta Physiol Scand Suppl 388:1–40
O’Brien RA, Ostberg AJ, Vrbová G (1978) Observations on the elimination of polyneuronal innervation in developing mammalian skeletal muscle. J Physiol 282:571–582. https://doi.org/10.1113/jphysiol.1978.sp012482
O’Kusky JR (1998) Postnatal changes in the numerical density and total number of asymmetric and symmetric synapses in the hypoglossal nucleus of the rat. Brain Res Dev Brain Res 108:179–191. https://doi.org/10.1016/s0165-3806(98)00048-0
O’Kusky J, Colonnier M (1982) Postnatal changes in the number of neurons and synapses in the visual cortex (area 17) of the macaque monkey: a stereological analysis in normal and monocularly deprived animals. J Comp Neurol 210:291–306. https://doi.org/10.1002/cne.902100308
Ofer N, Berger DR, Kasthuri N, Lichtman JW, Yuste R (2021) Ultrastructural analysis of dendritic spine necks reveals a continuum of spine morphologies. Dev Neurobiol 81:746–757. https://doi.org/10.1002/dneu.22829
Ofer N, Benavides-Piccione R, DeFelipe J, Yuste R (2022) Structural analysis of human and mouse dendritic spines reveals a morphological continuum and differences across ages and species. eNeuro 9. https://doi.org/10.1523/ENEURO.0039-22.2022
Oga T, Aoi H, Sasaki T, Fujita I, Ichinohe N (2013) Postnatal development of layer III pyramidal cells in the primary visual, inferior temporal, and prefrontal cortices of the marmoset. Front Neural Circuits 7:31. https://doi.org/10.3389/fncir.2013.00031
Oga T, Elston GN, Fujita I (2017) Postnatal dendritic growth and spinogenesis of layer-V pyramidal cells differ between visual, inferotemporal, and prefrontal cortex of the macaque monkey. Front Neurosci 11:118. https://doi.org/10.3389/fnins.2017.00118
Ohtaka-Maruyama C (2020) Subplate neurons as an organizer of mammalian neocortical development. Front Neuroanat 14:8. https://doi.org/10.3389/fnana.2020.00008
Okabe S (2009) Dendritic growth. In: Binder MD, Hirokawa N, Windhorst U (eds) Encyclopedia of neuroscience. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 937–942
Oppenheim RW (1991) Cell death during development of the nervous system. Annu Rev Neurosci 14:453–501. https://doi.org/10.1146/annurev.ne.14.030191.002321
Ozcan AS (2017) Filopodia: a rapid structural plasticity substrate for fast learning. Front Synaptic Neurosci 9:12. https://doi.org/10.3389/fnsyn.2017.00012
Palay SL (1956) Synapses in the central nervous system. J Biophys Biochem Cytol 2:193–202. https://doi.org/10.1083/jcb.2.4.193
Pan Y, Monje M (2020) Activity shapes neural circuit form and function: a historical perspective. J Neurosci 40:944–954. https://doi.org/10.1523/JNEUROSCI.0740-19.2019
Pchitskaya E, Bezprozvanny I (2020) Dendritic spines shape analysis-classification or clusterization? Perspective. Front Synaptic Neurosci 12:31. https://doi.org/10.3389/fnsyn.2020.00031
Pease SE, Segal RA (2014) Preserve and protect: maintaining axons within functional circuits. Trends Neurosci 37:572–582. https://doi.org/10.1016/j.tins.2014.07.007
Pendl SL, Salzwedel AP, Goldman BD, Barrett LF, Lin W, Gilmore JH, Gao W (2017) Emergence of a hierarchical brain during infancy reflected by stepwise functional connectivity. Hum Brain Mapp 38:2666–2682. https://doi.org/10.1002/hbm.23552
Pérez-Ortega J, Alejandre-García T, Yuste R (2021) Long-term stability of cortical ensembles. Elife 10. https://doi.org/10.7554/eLife.64449
Personius KE, Slusher BS, Udin SB (2016) Neuromuscular NMDA receptors modulate developmental synapse elimination. J Neurosci 36:8783–8789. https://doi.org/10.1523/JNEUROSCI.1181-16.2016
Petanjek Z, Judas M, Kostović I, Uylings HBM (2008) Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. Cereb Cortex 18:915–929. https://doi.org/10.1093/cercor/bhm124
Petanjek Z, Judaš M, Šimic G, Rasin MR, Uylings HBM, Rakic P, Kostovic I (2011) Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci U S A 108:13281–13286. https://doi.org/10.1073/pnas.1105108108
Petanjek Z, Sedmak D, Džaja D, Hladnik A, Rašin MR, Jovanov-Milosevic N (2019) The protracted maturation of associative layer IIIC pyramidal neurons in the human prefrontal cortex during childhood: a major role in cognitive development and selective alteration in autism. Front Psychiatry 10:122. https://doi.org/10.3389/fpsyt.2019.00122
Peters A (1987) Number of neurons and synapses in primary visual cortex. In: Jones EG, Peters A (eds) Cerebral cortex, vol 6. Springer US, Boston, pp 267–294
Peters A, Rosene DL (2003) In aging, is it gray or white? J Comp Neurol 462:139–143. https://doi.org/10.1002/cne.10715
Pettmann B, Henderson CE (1998) Neuronal cell death. Neuron 20:633–647. https://doi.org/10.1016/s0896-6273(00)81004-1
Peyton C, Einspieler C, Fjørtoft T, Adde L, Schreiber MD, Drobyshevsky A, Marks JD (2020) Correlates of normal and abnormal general movements in infancy and long-term neurodevelopment of preterm infants: insights from functional connectivity studies at term equivalence. J Clin Med 9. https://doi.org/10.3390/jcm9030834
Piekarski DJ, Johnson CM, Boivin JR, Thomas AW, Lin WC, Delevich K, Galarce EM, Wilbrecht L (2017) Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? Brain Res 1654:123–144. https://doi.org/10.1016/j.brainres.2016.08.042
Polese D, Riccio ML, Fagioli M, Mazzetta A, Fagioli F, Parisi P, Fagioli M (2022) The newborn’s reaction to light as the determinant of the brain’s activation at human birth. Front Integr Neurosci 16:933426. https://doi.org/10.3389/fnint.2022.933426
Pollen AA, Nowakowski TJ, Chen J, Retallack H, Sandoval-Espinosa C, Nicholas CR, Shuga J, Liu SJ, Oldham MC, Diaz A, Lim DA, Leyrat AA, West JA, Kriegstein AR (2015) Molecular identity of human outer radial glia during cortical development. Cell 163:55–67. https://doi.org/10.1016/j.cell.2015.09.004
Pollen AA, Kilik U, Lowe CB, Camp JG (2023) Human-specific genetics: new tools to explore the molecular and cellular basis of human evolution. Nat Rev Genet:1–25. https://doi.org/10.1038/s41576-022-00568-4
Poo MM, Pignatelli M, Ryan TJ, Tonegawa S, Bonhoeffer T, Martin KC, Rudenko A, Tsai LH, Tsien RW, Fishell G, Mullins C, Gonçalves JT, Shtrahman M, Johnston ST, Gage FH, Dan Y, Long J, Buzsáki G, Stevens C (2016) What is memory? The present state of the engram. BMC Biol 14:40. https://doi.org/10.1186/s12915-016-0261-6
Prechtl HF, Hopkins B (1986) Developmental transformations of spontaneous movements in early infancy. Early Hum Dev 14:233–238. https://doi.org/10.1016/0378-3782(86)90184-2
Preuss TM, Wise SP (2022) Evolution of prefrontal cortex. Neuropsychopharmacology 47:3–19. https://doi.org/10.1038/s41386-021-01076-5
Provenzi L, Lindstedt J, de Coen K, Gasparini L, Peruzzo D, Grumi S, Arrigoni F, Ahlqvist-Björkroth S (2021) The paternal brain in action: a review of human fathers’ fMRI brain responses to child-related stimuli. Brain Sci 11. https://doi.org/10.3390/brainsci11060816
Provis JM, van Driel D, Billson FA, Russell P (1985) Human fetal optic nerve: overproduction and elimination of retinal axons during development. J Comp Neurol 238:92–100. https://doi.org/10.1002/cne.902380108
Ptak R, Doganci N, Bourgeois A (2021) From action to cognition: neural reuse, network theory and the emergence of higher cognitive functions. Brain Sci 11. https://doi.org/10.3390/brainsci11121652
Purpura DP (1975) Normal and aberrant neuronal development in the cerebral cortex of human fetus and young infant. UCLA Forum Med Sci:141–169. https://doi.org/10.1016/b978-0-12-139050-1.50014-8
Purves D, Lichtman JW (1980) Elimination of synapses in the developing nervous system. Science 210:153–157. https://doi.org/10.1126/science.7414326
Quartz SR, Sejnowski TJ (1997) The neural basis of cognitive development: a constructivist manifesto. Behav Brain Sci 20:537–556. https://doi.org/10.1017/s0140525x97001581. discussion 556–96
Rakic P (2009) Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci 10:724–735. https://doi.org/10.1038/nrn2719
Rakic P, Riley KP (1983a) Overproduction and elimination of retinal axons in the fetal rhesus monkey. Science 219:1441–1444. https://doi.org/10.1126/science.6828871
Rakic P, Riley KP (1983b) Regulation of axon number in primate optic nerve by prenatal binocular competition. Nature 305:135–137. https://doi.org/10.1038/305135a0
Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS (1986) Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232:232–235. https://doi.org/10.1126/science.3952506
Rakic P, Bourgeois JP, Goldman-Rakic PS (1994) Synaptic development of the cerebral cortex: implications for learning, memory, and mental illness. Prog Brain Res 102:227–243. https://doi.org/10.1016/S0079-6123(08)60543-9
Ramos SI, Mussa ZM, Falk EN, Pai B, Giotti B, Allette K, Cai P, Dekio F, Sebra R, Beaumont KG, Tsankov AM, Tsankova NM (2022) An atlas of late prenatal human neurodevelopment resolved by single-nucleus transcriptomics. Nat Commun 13:7671. https://doi.org/10.1038/s41467-022-34975-2
Rangamani P, Levy MG, Khan S, Oster G (2016) Paradoxical signaling regulates structural plasticity in dendritic spines. Proc Natl Acad Sci U S A 113:E5298–E5307. https://doi.org/10.1073/pnas.1610391113
Rao-Ruiz P, Visser E, Mitrić M, Smit AB, van den Oever MC (2021) A synaptic framework for the persistence of memory engrams. Front Synaptic Neurosci 13:661476. https://doi.org/10.3389/fnsyn.2021.661476
Rasia-Filho AA (2022) Unraveling brain microcircuits, dendritic spines, and synaptic processing using multiple complementary approaches. Front Physiol 13:831568. https://doi.org/10.3389/fphys.2022.831568
Rasia-Filho AA, Guerra KTK, Vásquez CE, Dall’Oglio A, Reberger R, Jung CR, Calcagnotto ME (2021) The subcortical-allocortical- neocortical continuum for the emergence and morphological heterogeneity of pyramidal neurons in the human brain. Front Synaptic Neurosci 13:616607. https://doi.org/10.3389/fnsyn.2021.616607
Rasia-Filho AA, Calcagnotto ME, von Bohlen und Halbach O (2023a) Introduction: what are dendritic spines? In: Rasia-Filho AA et al (eds) Dendritic spines. Springer, Cham
Rasia-Filho AA, Calcagnotto ME, von Bohlen und Halbach O (2023b) Glial cell modulation of dendritic spine structure and synaptic function. In: Rasia-Filho AA et al (eds) Dendritic spines. Springer, Cham
Ray A, Christian JA, Mosso MB, Park E, Wegner W, Willig KI, Barth AL (2023) Quantitative fluorescence analysis reveals dendrite-specific thalamocortical plasticity in L5 pyramidal neurons during learning. J Neurosci 43:584–600. https://doi.org/10.1523/JNEUROSCI.1372-22.2022
Reberger R, Dall’Oglio A, Jung CR, Rasia-Filho AA (2018) Structure and diversity of human dendritic spines evidenced by a new three-dimensional reconstruction procedure for Golgi staining and light microscopy. J Neurosci Methods 293:27–36. https://doi.org/10.1016/j.jneumeth.2017.09.001
Redfern PA (1970) Neuromuscular transmission in new-born rats. J Physiol 209:701–709. https://doi.org/10.1113/jphysiol.1970.sp009187
Renner J, Rasia-Filho AA (2023) Morphological features of human dendritic spines. In: Rasia-Filho AA et al (eds) Dendritic spines. Springer, Cham
Riccomagno MM, Kolodkin AL (2015) Sculpting neural circuits by axon and dendrite pruning. Annu Rev Cell Dev Biol 31:779–805. https://doi.org/10.1146/annurev-cellbio-100913-013038
Ridge RM, Betz WJ (1984) The effect of selective, chronic stimulation on motor unit size in developing rat muscle. J Neurosci 4:2614–2620. https://doi.org/10.1523/JNEUROSCI.04-10-02614.1984
Rodríguez Cruz PM, Cossins J, Beeson D, Vincent A (2020) The neuromuscular junction in health and disease: molecular mechanisms governing synaptic formation and homeostasis. Front Mol Neurosci 13:610964. https://doi.org/10.3389/fnmol.2020.610964
Rosen BQ, Halgren E (2022) An estimation of the absolute number of axons indicates that human cortical areas are sparsely connected. PLoS Biol 20:e3001575. https://doi.org/10.1371/journal.pbio.3001575
Runge K, Cardoso C, de Chevigny A (2020) Dendritic spine plasticity: function and mechanisms. Front Synaptic Neurosci 12:36. https://doi.org/10.3389/fnsyn.2020.00036
Ryan TJ, Ortega-de San Luis C, Pezzoli M, Sen S (2021) Engram cell connectivity: an evolving substrate for information storage. Curr Opin Neurobiol 67:215–225. https://doi.org/10.1016/j.conb.2021.01.006
Sakai J (2020) Core concept: how synaptic pruning shapes neural wiring during development and, possibly, in disease. Proc Natl Acad Sci U S A 117:16096–16099. https://doi.org/10.1073/pnas.2010281117
Salamon I, Rasin M-R (2021) Evolution of the neocortex through RNA-binding proteins and post-transcriptional regulation. Front Neurosci 15:803107. https://doi.org/10.3389/fnins.2021.803107
Sasaki T, Aoi H, Oga T, Fujita I, Ichinohe N (2015) Postnatal development of dendritic structure of layer III pyramidal neurons in the medial prefrontal cortex of marmoset. Brain Struct Funct 220:3245–3258. https://doi.org/10.1007/s00429-014-0853-2
Schade JP, van Groenigen W (1961) Structural organization of the human cerebral cortex. 1. Maturation of the middle frontal gyrus. Acta Anat (Basel) 47:74–111. https://doi.org/10.1159/000141802
Schaeffer L, de Kerchove d’Exaerde A, Changeux JP (2001) Targeting transcription to the neuromuscular synapse. Neuron 31:15–22. https://doi.org/10.1016/S0896-6273(01)00353-1
Schwartz ML, Goldman-Rakic PS (1982) Single cortical neurones have axon collaterals to ipsilateral and contralateral cortex in fetal and adult primates. Nature 299:154–155. https://doi.org/10.1038/299154a0
Schwartz ML, Goldman-Rakic PS (1984) Callosal and intrahemispheric connectivity of the prefrontal association cortex in rhesus monkey: relation between intraparietal and principal sulcal cortex. J Comp Neurol 226:403–420. https://doi.org/10.1002/cne.902260309
Sedmak G, Judaš M (2021) White matter interstitial neurons in the adult human brain: 3% of cortical neurons in quest for recognition. Cell 10. https://doi.org/10.3390/cells10010190
Sedmak D, Hrvoj-Mihić B, Džaja D, Habek N, Uylings HB, Petanjek Z (2018) Biphasic dendritic growth of dorsolateral prefrontal cortex associative neurons and early cognitive development. Croat Med J 59:189–202. https://doi.org/10.3325/cmj.2018.59.189
Segal M (2017) Dendritic spines: morphological building blocks of memory. Neurobiol Learn Mem 138:3–9. https://doi.org/10.1016/j.nlm.2016.06.007
Selemon LD (2013) A role for synaptic plasticity in the adolescent development of executive function. Transl Psychiatry 3:e238. https://doi.org/10.1038/tp.2013.7
Selemon LD, Zecevic N (2015) Schizophrenia: a tale of two critical periods for prefrontal cortical development. Transl Psychiatry 5:e623. https://doi.org/10.1038/tp.2015.115
Semendeferi K, Teffer K, Buxhoeveden DP, Park MS, Bludau S, Amunts K, Travis K, Buckwalter J (2011) Spatial organization of neurons in the frontal pole sets humans apart from great apes. Cereb Cortex 21:1485–1497. https://doi.org/10.1093/cercor/bhq191
Seng C, Luo W, Földy C (2022) Circuit formation in the adult brain. Eur J Neurosci 56:4187–4213. https://doi.org/10.1111/ejn.15742
Shapiro LP, Parsons RG, Koleske AJ, Gourley SL (2017) Differential expression of cytoskeletal regulatory factors in the adolescent prefrontal cortex: implications for cortical development. J Neurosci Res 95:1123–1143. https://doi.org/10.1002/jnr.23960
Sharples SA, Miles GB (2021) Maturation of persistent and hyperpolarization-activated inward currents shapes the differential activation of motoneuron subtypes during postnatal development. Elife 10. https://doi.org/10.7554/eLife.71385
Shatz CJ, Stryker MP (1988) Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242:87–89. https://doi.org/10.1126/science.3175636
Sheng C, Javed U, Gibbs M, Long C, Yin J, Qin B, Yuan Q (2018) Experience-dependent structural plasticity targets dynamic filopodia in regulating dendrite maturation and synaptogenesis. Nat Commun 9:3362. https://doi.org/10.1038/s41467-018-05871-5
Shepherd GM (1996) The dendritic spine: a multifunctional integrative unit. J Neurophysiol 75:2197–2210. https://doi.org/10.1152/jn.1996.75.6.2197
Sherk H, Stryker MP (1976) Quantitative study of cortical orientation selectivity in visually inexperienced kitten. J Neurophysiol 39:63–70. https://doi.org/10.1152/jn.1976.39.1.63
Sheynikhovich D, Otani S, Bai J, Arleo A (2022) Long-term memory, synaptic plasticity and dopamine in rodent medial prefrontal cortex: role in executive functions. Front Behav Neurosci 16:1068271. https://doi.org/10.3389/fnbeh.2022.1068271
Sin WC, Haas K, Ruthazer ES, Cline HT (2002) Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 419:475–480. https://doi.org/10.1038/nature00987
Sohn J, Suzuki M, Youssef M, Hatada S, Larkum ME, Kawaguchi Y, Kubota Y (2022) Presynaptic supervision of cortical spine dynamics in motor learning. Sci Adv 8:eabm0531. https://doi.org/10.1126/sciadv.abm0531
Somel M, Franz H, Yan Z, Lorenc A, Guo S, Giger T, Kelso J, Nickel B, Dannemann M, Bahn S, Webster MJ, Weickert CS, Lachmann M, Pääbo S, Khaitovich P (2009) Transcriptional neoteny in the human brain. Proc Natl Acad Sci U S A 106:5743–5748. https://doi.org/10.1073/pnas.0900544106
Somel M, Liu X, Khaitovich P (2013) Human brain evolution: transcripts, metabolites and their regulators. Nat Rev Neurosci 14:112–127. https://doi.org/10.1038/nrn3372
Sousa SS, Amaro E, Crego A, Gonçalves ÓF, Sampaio A (2018) Developmental trajectory of the prefrontal cortex: a systematic review of diffusion tensor imaging studies. Brain Imaging Behav 12:1197–1210. https://doi.org/10.1007/s11682-017-9761-4
Spreafico R, Arcelli P, Frassoni C, Canetti P, Giaccone G, Rizzuti T, Mastrangelo M, Bentivoglio M (1999) Development of layer I of the human cerebral cortex after midgestation: architectonic findings, immunocytochemical identification of neurons and glia, and in situ labeling of apoptotic cells. J Comp Neurol 410:126–142. https://doi.org/10.1002/(sici)1096-9861(19990719)410:1<126:aid-cne11>3.0.co;2-5
Sretavan DW, Shatz CJ, Stryker MP (1988) Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336:468–471. https://doi.org/10.1038/336468a0
Stampanoni Bassi M, Iezzi E, Gilio L, Centonze D, Buttari F (2019) Synaptic plasticity shapes brain connectivity: implications for network topology. Int J Mol Sci 20. https://doi.org/10.3390/ijms20246193
Sun Y, Smirnov M, Kamasawa N, Yasuda R (2021) Rapid ultrastructural changes in the PSD and surrounding membrane after induction of structural LTP in single dendritic spines. J Neurosci 41:7003–7014. https://doi.org/10.1523/JNEUROSCI.1964-20.2021
Sunesen M, Changeux JP (2003) Transcription in neuromuscular junction formation: who turns on whom? J Neurocytol 32:677–684. https://doi.org/10.1023/B:NEUR.0000020616.53664.80
Supèr H, Soriano E, Uylings HB (1998) The functions of the preplate in development and evolution of the neocortex and hippocampus. Brain Res Brain Res Rev 27:40–64. https://doi.org/10.1016/s0165-0173(98)00005-8
Sweis BM, Mau W, Rabinowitz S, Cai DJ (2021) Dynamic and heterogeneous neural ensembles contribute to a memory engram. Curr Opin Neurobiol 67:199–206. https://doi.org/10.1016/j.conb.2020.11.017
Sydnor VJ, Larsen B, Bassett DS, Alexander-Bloch A, Fair DA, Liston C, Mackey AP, Milham MP, Pines A, Roalf DR, Seidlitz J, Xu T, Raznahan A, Satterthwaite TD (2021) Neurodevelopment of the association cortices: patterns, mechanisms, and implications for psychopathology. Neuron 109:2820–2846. https://doi.org/10.1016/j.neuron.2021.06.016
Takashima S, Chan F, Becker LE, Armstrong DL (1980) Morphology of the developing visual cortex of the human infant: a quantitative and qualitative Golgi study. J Neuropathol Exp Neurol 39:487–501. https://doi.org/10.1097/00005072-198007000-00007
Tamnes CK, Herting MM, Goddings A-L, Meuwese R, Blakemore S-J, Dahl RE, Güroğlu B, Raznahan A, Sowell ER, Crone EA, Mills KL (2017) Development of the cerebral cortex across adolescence: a multisample study of inter-related longitudinal changes in cortical volume, surface area, and thickness. J Neurosci 37:3402–3412. https://doi.org/10.1523/JNEUROSCI.3302-16.2017
Tau GZ, Peterson BS (2010) Normal development of brain circuits. Neuropsychopharmacology 35:147–168. https://doi.org/10.1038/npp.2009.115
Teffer K, Semendeferi K (2012) Human prefrontal cortex: evolution, development, and pathology. Prog Brain Res 195:191–218. https://doi.org/10.1016/B978-0-444-53860-4.00009-X
Thompson W (1983) Synapse elimination in neonatal rat muscle is sensitive to pattern of muscle use. Nature 302:614–616. https://doi.org/10.1038/302614a0
Thompson W, Jansen JK (1977) The extent of sprouting of remaining motor units in partly denervated immature and adult rat soleus muscle. Neuroscience 2:523–535. https://doi.org/10.1016/0306-4522(77)90049-5
Thompson W, Kuffler DP, Jansen JK (1979) The effect of prolonged, reversible block of nerve impulses on the elimination of polyneuronal innervation of new-born rat skeletal muscle fibers. Neuroscience 4:271–281. https://doi.org/10.1016/0306-4522(79)90088-5
Thompson WJ, Sutton LA, Riley DA (1984) Fibre type composition of single motor units during synapse elimination in neonatal rat soleus muscle. Nature 309:709–711. https://doi.org/10.1038/309709a0
Tolonen M, Palva JM, Andersson S, Vanhatalo S (2007) Development of the spontaneous activity transients and ongoing cortical activity in human preterm babies. Neuroscience 145:997–1006. https://doi.org/10.1016/j.neuroscience.2006.12.070
Tomàs J, Lanuza MA, Santafé MM, Cilleros-Mañé V, Just-Borràs L, Balanyà-Segura M, Polishchuk A, Nadal L, Tomàs M, Garcia N (2023) Muscarinic receptors in developmental axonal competition at the neuromuscular junction. Mol Neurobiol 60:1580–1593. https://doi.org/10.1007/s12035-022-03154-1
Tong R, Emptage NJ, Padamsey Z (2020) A two-compartment model of synaptic computation and plasticity. Mol Brain 13:79. https://doi.org/10.1186/s13041-020-00617-1
Tønnesen J, Nägerl UV (2016) Dendritic spines as tunable regulators of synaptic signals. Front Psychiatry 7:101. https://doi.org/10.3389/fpsyt.2016.00101
Tousignant B, Eugène F, Sirois K, Jackson PL (2018) Difference in neural response to social exclusion observation and subsequent altruism between adolescents and adults. Neuropsychologia 116:15–25. https://doi.org/10.1016/j.neuropsychologia.2017.04.017
Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420:788–794. https://doi.org/10.1038/nature01273
Tropea D, Majewska AK, Garcia R, Sur M (2010) Structural dynamics of synapses in vivo correlate with functional changes during experience-dependent plasticity in visual cortex. J Neurosci 30:11086–11095. https://doi.org/10.1523/JNEUROSCI.1661-10.2010
Ucar H, Watanabe S, Noguchi J, Morimoto Y, Iino Y, Yagishita S, Takahashi N, Kasai H (2021) Mechanical actions of dendritic-spine enlargement on presynaptic exocytosis. Nature 600:686–689. https://doi.org/10.1038/s41586-021-04125-7
Uylings HBM (2006) Development of the human cortex and the concept of “critical” or “sensitive” periods. Lang Learn 56:59–90. https://doi.org/10.1111/j.1467-9922.2006.00355.x
Uylings HBM, de Brabander JM (2002) Neuronal changes in normal human aging and Alzheimer’s disease. Brain Cogn 49:268–276. https://doi.org/10.1006/brcg.2001.1500
Uylings HBM, van Pelt J, Parnavelas JG, Ruiz-Marcos A (1994) Geometrical and topological characteristics in the dendritic development of cortical pyramidal and non-pyramidal neurons. Prog Brain Res 102:109–123. https://doi.org/10.1016/s0079-6123(08)60535-x
van Pelt J, Uylings HBM (2002) Branching rates and growth functions in the outgrowth of dendritic branching patterns. Network 13:261–281. https://doi.org/10.1088/0954-898x/13/3/302
Vanderhaeghen P, Polleux F (2023) Developmental mechanisms underlying the evolution of human cortical circuits. Nat Rev Neurosci. https://doi.org/10.1038/s41583-023-00675-z
Vardalaki D, Chung K, Harnett MT (2022) Filopodia are a structural substrate for silent synapses in adult neocortex. Nature 612:323–327. https://doi.org/10.1038/s41586-022-05483-6
Vasalauskaite A, Morgan JE, Sengpiel F (2019) Plasticity in adult mouse visual cortex following optic nerve injury. Cereb Cortex 29:1767–1777. https://doi.org/10.1093/cercor/bhy347
Vasung L, Lepage C, Radoš M, Pletikos M, Goldman JS, Richiardi J, Raguž M, Fischi-Gómez E, Karama S, Huppi PS, Evans AC, Kostovic I (2016) Quantitative and qualitative analysis of transient fetal compartments during prenatal human brain development. Front Neuroanat 10:11. https://doi.org/10.3389/fnana.2016.00011
Vasung L, Raguz M, Kostovic I, Takahashi E (2017) Spatiotemporal relationship of brain pathways during human fetal development using high-angular resolution diffusion MR imaging and histology. Front Neurosci 11:348. https://doi.org/10.3389/fnins.2017.00348
Verney C (1999) Distribution of the catecholaminergic neurons in the central nervous system of human embryos and fetuses. Microsc Res Tech 46:24–47. https://doi.org/10.1002/(SICI)1097-0029(19990701)46:1%3C24:AID-JEMT3%3E3.0.CO;2-E
Verney C, Milosevic A, Alvarez C, Berger B (1993) Immunocytochemical evidence of well-developed dopaminergic and noradrenergic innervations in the frontal cerebral cortex of human fetuses at midgestation. J Comp Neurol 336:331–344. https://doi.org/10.1002/cne.903360303
Volzhenin K, Changeux JP, Dumas G (2022) Multilevel development of cognitive abilities in an artificial neural network. Proc Natl Acad Sci U S A 119:e2201304119. https://doi.org/10.1073/pnas.2201304119
von Bohlen und Halbach O (2023) Neurotrophic factors and dendritic spines. In: Rasia-Filho AA et al (eds) Dendritic spines. Springer, Cham
Walsh MK, Lichtman JW (2003) In vivo time-lapse imaging of synaptic takeover associated with naturally occurring synapse elimination. Neuron 37:67–73. https://doi.org/10.1016/s0896-6273(02)01142-x
Wang L, Conner JM, Rickert J, Tuszynski MH (2011) Structural plasticity within highly specific neuronal populations identifies a unique parcellation of motor learning in the adult brain. Proc Natl Acad Sci U S A 108:2545–2550. https://doi.org/10.1073/pnas.1014335108
Weber JP, Andrásfalvy BK, Polito M, Magó Á, Ujfalussy BB, Makara JK (2016) Location-dependent synaptic plasticity rules by dendritic spine cooperativity. Nat Commun 7:11380. https://doi.org/10.1038/ncomms11380
Werchan DM, Amso D (2017) A novel ecological account of prefrontal cortex functional development. Psychol Rev 124:720–739. https://doi.org/10.1037/rev0000078
Wess JM, Isaiah A, Watkins PV, Kanold PO (2017) Subplate neurons are the first cortical neurons to respond to sensory stimuli. Proc Natl Acad Sci U S A 114:12602–12607. https://doi.org/10.1073/pnas.1710793114
White LD, Barone S (2001) Qualitative and quantitative estimates of apoptosis from birth to senescence in the rat brain. Cell Death Differ 8:345–356. https://doi.org/10.1038/sj.cdd.4400816
Whitford KL, Dijkhuizen P, Polleux F, Ghosh A (2002) Molecular control of cortical dendrite development. Annu Rev Neurosci 25:127–149. https://doi.org/10.1146/annurev.neuro.25.112701.142932
Wiesel TN, Hubel DH (1963a) Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. J Neurophysiol 26:978–993. https://doi.org/10.1152/jn.1963.26.6.978
Wiesel TN, Hubel DH (1963b) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 26:1003–1017. https://doi.org/10.1152/jn.1963.26.6.1003
Wilbrecht L, Holtmaat A, Wright N, Fox K, Svoboda K (2010) Structural plasticity underlies experience-dependent functional plasticity of cortical circuits. J Neurosci 30:4927–4932. https://doi.org/10.1523/JNEUROSCI.6403-09.2010
Wildenberg G, Li H, Kasthuri N (2023) The development of synapses in mouse and macaque primary sensory cortices. bioRxiv. https://doi.org/10.1101/2023.02.15.528564
Williams RW, Rakic P (1988) Elimination of neurons from the rhesus monkey’s lateral geniculate nucleus during development. J Comp Neurol 272:424–436. https://doi.org/10.1002/cne.902720310
Winfield DA, Rivera-Dominguez M, Powell TP (1982) The termination of geniculocortical fibres in area 17 of the visual cortex in the macaque monkey. Brain Res 231:19–32. https://doi.org/10.1016/0006-8993(82)90004-x
Won H, Huang J, Opland CK, Hartl CL, Geschwind DH (2019) Human evolved regulatory elements modulate genes involved in cortical expansion and neurodevelopmental disease susceptibility. Nat Commun 10:2396. https://doi.org/10.1038/s41467-019-10248-3
Wong FK, Marín O (2019) Developmental cell death in the cerebral cortex. Annu Rev Cell Dev Biol 35:523–542. https://doi.org/10.1146/annurev-cellbio-100818-125204
Wouterlood FG (2023) Techniques to render dendritic spines visible in the microscope. In: Rasia-Filho AA et al (eds) Dendritic spines. Springer, Cham
Wright LL, Cunningham TJ, Smolen AJ (1983) Developmental neuron death in the rat superior cervical sympathetic ganglion: cell counts and ultrastructure. J Neurocytol 12:727–738. https://doi.org/10.1007/BF01258147
Wu H, Xiong WC, Mei L (2010) To build a synapse: signaling pathways in neuromuscular junction assembly. Development 137:1017–1033. https://doi.org/10.1242/dev.038711
Wyatt RM, Balice-Gordon RJ (2003) Activity-dependent elimination of neuromuscular synapses. J Neurocytol 32:777–794. https://doi.org/10.1023/B:NEUR.0000020623.62043.33
Xu T, Yu X, Perlik AJ, Tobin WF, Zweig JA, Tennant K, Jones T, Zuo Y (2009) Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462:915–919. https://doi.org/10.1038/nature08389
Xu R, Bichot NP, Takahashi A, Desimone R (2022a) The cortical connectome of primate lateral prefrontal cortex. Neuron 110:312–327.e7. https://doi.org/10.1016/j.neuron.2021.10.018
Xu J, Zhu J, Li Y, Yao Y, Xuan A, Li D, Yu T, Zhu D (2022b) Three-dimensional mapping reveals heterochronic development of the neuromuscular system in postnatal mouse skeletal muscles. Commun Biol 5:1200. https://doi.org/10.1038/s42003-022-04159-1
Yamaguchi Y, Miura M (2015) Programmed cell death in neurodevelopment. Dev Cell 32:478–490. https://doi.org/10.1016/j.devcel.2015.01.019
Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM, Birchmeier C, Burden SJ (2001a) Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30:399–410. https://doi.org/10.1016/S0896-6273(01)00287-2
Yang JF, Cao G, Koirala S, Reddy LV, Ko CP (2001b) Schwann cells express active agrin and enhance aggregation of acetylcholine receptors on muscle fibers. J Neurosci 21:9572–9584. https://doi.org/10.1523/jneurosci.21-24-09572.2001
Yang G, Pan F, Gan W-B (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462:920–924. https://doi.org/10.1038/nature08577
Yeterian EH, Pandya DN (1994) Laminar origin of striatal and thalamic projections of the prefrontal cortex in rhesus monkeys. Exp Brain Res 99:383–398. https://doi.org/10.1007/BF00228975
Yin W, Chen M-H, Hung S-C, Baluyot KR, Li T, Lin W (2019) Brain functional development separates into three distinct time periods in the first two years of life. Neuroimage 189:715–726. https://doi.org/10.1016/j.neuroimage.2019.01.025
Yoshihara Y, de Roo M, Muller D (2009) Dendritic spine formation and stabilization. Curr Opin Neurobiol 19:146–153. https://doi.org/10.1016/j.conb.2009.05.013
Yuste R (2015) The discovery of dendritic spines by Cajal. Front Neuroanat 9:18. https://doi.org/10.3389/fnana.2015.00018
Yuste R, Bonhoeffer T (2004) Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci 5:24–34. https://doi.org/10.1038/nrn1300
Zecevic N (1998) Synaptogenesis in layer I of the human cerebral cortex in the first half of gestation. Cereb Cortex 8:245–252. https://doi.org/10.1093/cercor/8.3.245
Zecevic N, Rakic P (1991) Synaptogenesis in monkey somatosensory cortex. Cereb Cortex 1:510–523. https://doi.org/10.1093/cercor/1.6.510
Zecevic N, Rakic P (2001) Development of layer I neurons in the primate cerebral cortex. J Neurosci 21:5607–5619. https://doi.org/10.1523/JNEUROSCI.21-15-05607.2001
Zecevic N, Verney C (1995) Development of the catecholamine neurons in human embryos and fetuses, with special emphasis on the innervation of the cerebral cortex. J Comp Neurol 351:509–535. https://doi.org/10.1002/cne.903510404
Zecevic N, Bourgeois JP, Rakic P (1989) Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. Brain Res Dev Brain Res 50:11–32. https://doi.org/10.1016/0165-3806(89)90124-7
Zecevic N, Milosevic A, Rakic S, Marín-Padilla M (1999) Early development and composition of the human primordial plexiform layer: an immunohistochemical study. J Comp Neurol 412:241–254
Zempo B, Yamamoto Y, Williams T, Ono F (2020) Synaptic silencing of fast muscle is compensated by rewired innervation of slow muscle. Sci Adv 6:eaax8382. https://doi.org/10.1126/sciadv.aax8382
Zielinski BS, Hendrickson AE (1992) Development of synapses in macaque monkey striate cortex. Vis Neurosci 8:491–504. https://doi.org/10.1017/s0952523800005599
Zikopoulos B, Barbas H (2013) Altered neural connectivity in excitatory and inhibitory cortical circuits in autism. Front Hum Neurosci 7:609. https://doi.org/10.3389/fnhum.2013.00609
Zimmermann KS, Richardson R, Baker KD (2019) Maturational changes in prefrontal and amygdala circuits in adolescence: implications for understanding fear inhibition during a vulnerable period of development. Brain Sci 9. https://doi.org/10.3390/brainsci9030065
Ziv NE, Smith SJ (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91–102. https://doi.org/10.1016/s0896-6273(00)80283-4
Zuo Y, Lin A, Chang P, Gan W-B (2005a) Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46:181–189. https://doi.org/10.1016/j.neuron.2005.04.001
Zuo Y, Yang G, Kwon E, Gan W-B (2005b) Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436:261–265. https://doi.org/10.1038/nature03715
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Petanjek, Z., Banovac, I., Sedmak, D., Hladnik, A. (2023). Dendritic Spines: Synaptogenesis and Synaptic Pruning for the Developmental Organization of Brain Circuits. In: Rasia-Filho, A.A., Calcagnotto, M.E., von Bohlen und Halbach, O. (eds) Dendritic Spines. Advances in Neurobiology, vol 34. Springer, Cham. https://doi.org/10.1007/978-3-031-36159-3_4
Download citation
DOI: https://doi.org/10.1007/978-3-031-36159-3_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-36158-6
Online ISBN: 978-3-031-36159-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)