Abstract
The classical theory of cortical systematic variation has been independently described in reptiles, monotremes, marsupials and placental mammals, including primates, suggesting a common bauplan in the evolution of the cortex. The Structural Model is based on the systematic variation of the cortex and is a platform for advancing testable hypotheses about cortical organization and function across species, including humans. The Structural Model captures the overall laminar structure of areas by dividing the cortical architectonic continuum into discrete categories (cortical types), which can be used to test hypotheses about cortical organization. By type, the phylogenetically ancient limbic cortices—which form a ring at the base of the cerebral hemisphere—are agranular if they lack layer IV, or dysgranular if they have an incipient granular layer IV. Beyond the dysgranular areas, eulaminate type cortices have six layers. The number and laminar elaboration of eulaminate areas differ depending on species or cortical system within a species. The construct of cortical type retains the topology of the systematic variation of the cortex and forms the basis for a predictive Structural Model, which has successfully linked cortical variation to the laminar pattern and strength of cortical connections, the continuum of plasticity and stability of areas, the regularities in the distribution of classical and novel markers, and the preferential vulnerability of limbic areas to neurodegenerative and psychiatric diseases. The origin of cortical types has been recently traced to cortical development, and helps explain the variability of diseases with an onset in ontogeny.
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[Note: this figure is a re-examination of material from an earlier paper (Reillo et al. 2011)]
[Note: this figure is an examination of material from a gift of Dr. Alan Peters]
[Note: this figure is an examination of material from a gift of Dr. Alan Peters]
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References
Abbie AA (1940) Cortical lamination in the monotremata. J Comp Neurol 72:429–467
Abbie AA (1942) Cortical lamination in a polyprotodont marsupial, perameles nasuta. J Comp Neurol 76:509–536
Allman J (2000) Evolving brains. Scientific American Library, New York
Ariëns Kappers CU, Huber GC, Crosby EC (1936) The comparative anatomy of the nervous system of vertebrates, including man. Macmillan, New York
Arnold SE, Hyman BT, Flory J, Damasio AR, Van Hoesen GW (1991) The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer’s disease. Cereb Cortex 1:103–116
Badre D, D’Esposito M (2007) Functional magnetic resonance imaging evidence for a hierarchical organization of the prefrontal cortex. J Cogn Neurosci 19(12):2082–2099
Bailey P, von Bonin G (1951) The isocortex of man. University of Illinois Press, Urbana
Barbas H (1986) Pattern in the laminar origin of corticocortical connections. J Comp Neurol 252:415–422
Barbas H (1988) Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 276:313–342
Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci Biobehav Rev 19:499–510
Barbas H (2015) General Cortical and special Prefrontal Connections: Principles from Structure to Function. Annu Rev Neurosci 38:269–289
Barbas H, García-Cabezas MA (2015) Motor cortex layer 4: less is more. Trends Neurosci 38(5):259–261
Barbas H, García-Cabezas MA (2016) How the prefrontal executive got its stripes. Curr Opin Neurobiol 40:125–134. https://doi.org/10.1016/j.conb.2016.07.003
Barbas H, Pandya DN (1987) Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J Comp Neurol 256:211–218
Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286(3):353–375
Barbas H, Rempel-Clower N (1997) Cortical structure predicts the pattern of corticocortical connections. Cereb Cortex 7:635–646
Barbas H, Ghashghaei H, Dombrowski SM, Rempel-Clower NL (1999) Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey. J Comp Neurol 410:343–367
Barbas H, Hilgetag CC, Saha S, Dermon CR, Suski JL (2005a) Parallel organization of contralateral and ipsilateral prefrontal cortical projections in the rhesus monkey. BMC Neurosci 6(1):32
Barbas H, Medalla M, Alade O, Suski J, Zikopoulos B, Lera P (2005b) Relationship of prefrontal connections to inhibitory systems in superior temporal areas in the rhesus monkey. Cereb Cortex 15(9):1356–1370
Barbas H, Wang J, Joyce MKP, García-Cabezas MA (2018) Pathway mechanism for excitatory and inhibitory control in working memory. J Neurophysiol 120:2659–2678
Benowitz LI, Routtenberg A (1997) GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 20(2):84–91
Beul SF, Grant S, Hilgetag CC (2015) A predictive model of the cat cortical connectome based on cytoarchitecture and distance. Brain Struct Funct 220(6):3167–3184. https://doi.org/10.1007/s00429-014-0849-y
Beul SF, Barbas H, Hilgetag CC (2017) A predictive structural model of the primate connectome. Sci Rep 7:43176. https://doi.org/10.1038/srep43176
Borrell V, Reillo I (2012) Emerging roles of neural stem cells in cerebral cortex development and evolution. Dev Neurobiol 72(7):955–971. https://doi.org/10.1002/dneu.22013
Braak H (1980) Architectonics of the human telencephalic cortex. Studies of brain function, vol 4. Springer, Berlin; New York
Braak H, Del Tredici K (2018) Spreading of Tau Pathology in Sporadic Alzheimer’s disease along cortico-cortical top-down connections. Cereb Cortex 28(9):3372–3384. https://doi.org/10.1093/cercor/bhy152
Braak H, Bohl JR, Muller CM, Rub U, de Vos RA, Del Tredici K (2006) Stanley Fahn Lecture 2005: the staging procedure for the inclusion body pathology associated with sporadic Parkinson’s disease reconsidered. Movem Disord 21(12):2042–2051. https://doi.org/10.1002/mds.21065
Braitenberg V (1962) A note on myeloarchitectonics. J Comp Neurol 118:141–156
Brettschneider J, Del Tredici K, Lee VM, Trojanowski JQ (2015) Spreading of pathology in neurodegenerative diseases: a focus on human studies. Nat Rev Neurosci 16(2):109–120. https://doi.org/10.1038/nrn3887
Broca P (1878) Anatomie comparée des circonvolutions cérébrales: Le grand lobe limbique et la scissure limbique dans la série des mammifères. Revue D’anthropologie 1:385–498
Brodmann KG (1909/1999) Brodmann’s Localisation in the Cerebral Cortex. Translated from German by Laurence J. Imperial College Press, London
Burt JB, Demirtas M, Eckner WJ, Navejar NM, Ji JL, Martin WJ, Bernacchia A, Anticevic A, Murray JD (2018) Hierarchy of transcriptomic specialization across human cortex captured by structural neuroimagin topography. Nat Neurosci 9:1251–1259. https://doi.org/10.1038/s41593-018-0195-0
Bystron I, Blakemore C, Rakic P (2008) Development of the human cerebral cortex: boulder committee revisited. NatRevNeurosci 9(2):110–122
Cahalane DJ, Charvet CJ, Finlay BL (2012) Systematic, balancing gradients in neuron density and number across the primate isocortex. Front Neuroanat 6:28. https://doi.org/10.3389/fnana.2012.00028
Campbell AW (1905) Histological studies on the localisation of cerebral function. University Press, Cambridge
Campbell MJ, Morrison JH (1989) Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 282:191–205
Chanes L, Barrett LF (2016) Redefining the Role of Limbic Areas in Cortical Processing. Trends Cogn Sci 20(2):96–106. https://doi.org/10.1016/j.tics.2015.11.005
Damasio AR, Van Hoesen GW (1985) The limbic system and the localisation of herpes simplex encephalitis. J Neurol Neurosurg Psychiatry 48(4):297–301
Dart RA (1934) The dual structure of the neopallium: Its history and significance. J Anat 69:3–19
Darwin C (1859) On the origin of species by means of natural selection: or, The preservation of favoured races in the struggle for life. John Murray, Albemarle Street, London
Dehay C, Kennedy H, Kosik KS (2015) The outer subventricular zone and primate-specific cortical complexification. Neuron 85(4):683–694. https://doi.org/10.1016/j.neuron.2014.12.060
del Río-Hortega P (1934/1962) The microscopic anatomy of tumors of the central and peripheral nervous system. Thomas, Springfield, Ill.
Ding SL, Royall JJ, Sunkin SM, Ng L, Facer BA, Lesnar P, Guillozet-Bongaarts A, McMurray B, Szafer A, Dolbeare TA, Stevens A, Tirrell L, Benner T, Caldejon S, Dalley RA, Dee N, Lau C, Nyhus J, Reding M, Riley ZL, Sandman D, Shen E, van der Kouwe A, Varjabedian A, Wright M, Zollei L, Dang C, Knowles JA, Koch C, Phillips JW, Sestan N, Wohnoutka P, Zielke HR, Hohmann JG, Jones AR, Bernard A, Hawrylycz MJ, Hof PR, Fischl B, Lein ES (2016) Comprehensive cellular-resolution atlas of the adult human brain. J Comp Neurol 524(16):3127–3481. https://doi.org/10.1002/cne.24080
Dombrowski SM, Hilgetag CC, Barbas H (2001) Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. Cereb Cortex 11:975–988
Duyckaerts C, Colle MA, Dessi F, Piette F, Hauw JJ (1998) Progression of Alzheimer histopathological changes. Acta neurologica Belgica 98(2):180–185
Elston GN (2003) Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. Cereb Cortex 13(11):1124–1138
Elston GN, Benavides-Piccione R, DeFelipe J (2005) A study of pyramidal cell structure in the cingulate cortex of the macaque monkey with comparative notes on inferotemporal and primary visual cortex. Cereb Cortex 15(1):64–73
Ercsey-Ravasz M, Markov NT, Lamy C, Van Essen DC, Knoblauch K, Toroczkai Z, Kennedy H (2013) A predictive network model of cerebral cortical connectivity based on a distance rule. Neuron 80(1):184–197. https://doi.org/10.1016/j.neuron.2013.07.036
Fame RM, Dehay C, Kennedy H, Macklis JD (2017) Subtype-specific genes that characterize subpopulations of callosal projection neurons in mouse identify molecularly homologous populations in macaque cortex. Cereb Cortex 27(3):1817–1830. https://doi.org/10.1093/cercor/bhw023
Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47
Filimonoff IN (1947) A rational subdivision of the cerebral cortex. Arch Neurol Psychiat 58:296–311
Galaburda A, Sanides F (1980) Cytoarchitectonic organization of the human auditory cortex. J Comp Neurol 190:597–610
Garcia-Cabezas MA, Joyce MP, John Y, Zikopoulos B, Barbas H (2017) Mirror trends of plasticity and stability indicators in primate prefrontal cortex. Eur J Neurosci 46(8):2392–2405
García-Cabezas MA, Barbas H (2017) Anterior cingulate pathways may affect emotions through orbitofrontal cortex. Cereb Cortex 27(10):4891–4910. https://doi.org/10.1093/cercor/bhw284
García-Cabezas MA, Barbas H, Zikopoulos B (2018) Parallel development of chromatin patterns, neuron morphology, and connections: Potential for disruption in autism. Front Neuroanat 12:70. https://doi.org/10.3389/fnana.2018.00070
Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, Ugurbil K, Andersson J, Beckmann CF, Jenkinson M, Smith SM, Van Essen DC (2016) A multi-modal parcellation of human cerebral cortex. Nature 536(7615):171–178. https://doi.org/10.1038/nature18933
Gloor P, Olivier A, Quesney LF, Andermann F, Horowitz S (1982) The role of the limbic system in experiential phenomena of temporal lobe epilepsy. Ann Neurol 12:129–144
Goulas A, Uylings HB, Stiers P (2014) Mapping the hierarchical layout of the structural network of the macaque prefrontal cortex. Cereb Cortex 24(5):1178–1194. https://doi.org/10.1093/cercor/bhs399
Goulas A, Uylings HB, Hilgetag CC (2017) Principles of ipsilateral and contralateral cortico-cortical connectivity in the mouse. Brain Struct Funct 222(3):1281–1295. https://doi.org/10.1007/s00429-016-1277-y
Grant S, Hilgetag CC (2005) Graded classes of cortical connections: quantitative analyses of laminar projections to motion areas of cat extrastriate cortex. Eur J Neurosci 22(3):681–696
He Y, Chen ZJ, Evans AC (2007) Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb Cortex 17(10):2407–2419
Henssen A, Zilles K, Palomero-Gallagher N, Schleicher A, Mohlberg H, Gerboga F, Eickhoff SB, Bludau S, Amunts K (2016) Cytoarchitecture and probability maps of the human medial orbitofrontal cortex. Cortex 75:87–112. https://doi.org/10.1016/j.cortex.2015.11.006
Hilgetag CC, Grant S (2010) Cytoarchitectural differences are a key determinant of laminar projection origins in the visual cortex. NeuroImage 51(3):1006–1017. https://doi.org/10.1016/j.neuroimage.2010.03.006
Hilgetag CC, Medalla M, Beul S, Barbas H (2016) The primate connectome in context: principles of connections of the cortical visual system. NeuroImage 134:685–702. https://doi.org/10.1016/j.neuroimage.2016.04.017 doi
Hof PR, Mufson EJ, Morrison JH (1995) Human orbitofrontal cortex: cytoarchitecture and quantitative immunohistochemical parcellation. J Comp Neurol 359:48–68
Holmes MD, Brown M, Tucker DM (2004) Are “generalized” seizures truly generalized? Evidence of localized mesial frontal and frontopolar discharges in absence. Epilepsia 45(12):1568–1579. https://doi.org/10.1111/j.0013-9580.2004.23204.x
Hubel DH (1988) Eye, brain, and vision. Scientific American Library series, vol no 22. Scientific American Library: Distributed by W.H. Freeman, New York
Huntenburg JM, Bazin PL, Margulies DS (2018) Large-Scale Gradients in Human Cortical Organization. Trends Cogn Sci 22(1):21–31. https://doi.org/10.1016/j.tics.2017.11.002
Jacot-Descombes S, Uppal N, Wicinski B, Santos M, Schmeidler J, Giannakopoulos P, Heinsen H, Schmitz C, Hof PR (2012) Decreased pyramidal neuron size in Brodmann areas 44 and 45 in patients with autism. Acta Neuropathol 124(1):67–79. https://doi.org/10.1007/s00401-012-0976-6
Jones EG, Powell TPS (1970) An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93:793–820
Joyce MP, Barbas H (2018) Cortical connections position primate area 25 as a keystone for interoception, emotion, and memory. J Neurosci 38(7):1677–1698. https://doi.org/10.1523/JNEUROSCI.2363-17.2017
Kaas JH (2004) Evolution of somatosensory and motor cortex in primates. Anat Rec A Discov Mol Cell Evol Biol 281(1):1148–1156
Kapfhammer JP, Schwab ME (1994) Inverse patterns of myelination and GAP-43 expression in the adult CNS: neurite growth inhibitors as regulators of neuronal plasticity? J Comp Neurol 340(2):194–206
Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171(2):157–191
Lake BB, Chen S, Sos BC, Fan J, Kaeser GE, Yung YC, Duong TE, Gao D, Chun J, Kharchenko PV, Zhang K (2017) Integrative single-cell analysis of transcriptional and epigenetic states in the human adult brain. Nat Biotechnol. https://doi.org/10.1038/nbt.4038
LaMonica BE, Lui JH, Wang X, Kriegstein AR (2012) OSVZ progenitors in the human cortex: an updated perspective on neurodevelopmental disease. Curr Opin Neurobiol 22(5):747–753. https://doi.org/10.1016/j.conb.2012.03.006
Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M, Kennedy H, Dehay C (2005) G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47(3):353–364
Lukaszewicz A, Cortay V, Giroud P, Berland M, Smart I, Kennedy H, Dehay C (2006) The concerted modulation of proliferation and migration contributes to the specification of the cytoarchitecture and dimensions of cortical areas. Cereb Cortex 16(Suppl 1):i26–i34
Malikovic A, Amunts K, Schleicher A, Mohlberg H, Kujovic M, Palomero-Gallagher N, Eickhoff SB, Zilles K (2016) Cytoarchitecture of the human lateral occipital cortex: mapping of two extrastriate areas hOc4la and hOc4lp. Brain Struct Funct 221(4):1877–1897. https://doi.org/10.1007/s00429-015-1009-8
Martinez-Cerdeno V, Noctor SC (2016) Cortical evolution 2015: Discussion of neural progenitor cell nomenclature. J Comp Neurol 524(3):704–709. https://doi.org/10.1002/cne.23909
Martinez-Cerdeno V, Noctor SC (2018) Neural progenitor cell terminology. Front Neuroanat 12:104. https://doi.org/10.3389/fnana.2018.00104
Martinez-Cerdeno V, Cunningham CL, Camacho J, Antczak JL, Prakash AN, Cziep ME, Walker AI, Noctor SC (2012) Comparative analysis of the subventricular zone in rat, ferret and macaque: evidence for an outer subventricular zone in rodents. PLoS One 7(1):e30178. https://doi.org/10.1371/journal.pone.0030178
Maunsell JHR, Van Essen DC (1983) The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci 3:2563–2586
Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, Schwalb JM, Kennedy SH (2005) Deep brain stimulation for treatment-resistant depression. Neuron 45(5):651–660
Medalla M, Barbas H (2006) Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure. Eur J Neurosci 23(1):161–179
Medina L, Abellan A (2009) Development and evolution of the pallium. Semin Cell Dev Biol 20(6):698–711. https://doi.org/10.1016/j.semcdb.2009.04.008
Mesulam MM (1985) Patterns in behavioral neuroanatomy: Association areas, the limbic system, and hemispheric specialization. In: Mesulam MM (ed) Principles of behavioral neurology. F. A. Davis Company, Philadelphia, pp 1–70
Mesulam MM (1998) From sensation to cognition. Brain 121:1013–1052
Mesulam MM, Mufson EJ (1982) Insula of the old world monkey. I: Architectonics in the insulo- orbito-temporal component of the paralimbic brain. J Comp Neurol 212:1–22
Montiel JF, Aboitiz F (2015) Pallial patterning and the origin of the isocortex. Front Neurosci 9:377. https://doi.org/10.3389/fnins.2015.00377
Morgane PJ, Glezer II, Jacobs MS (1990) Comparative and evolutionary anatomy of the visual cortex of the dolphin. Cereb Cortex 8B:215–262
Nieuwenhuys R, Broere CA (2017) A map of the human neocortex showing the estimated overall myelin content of the individual architectonic areas based on the studies of Adolf Hopf. Brain Struct Funct 222(1):465–480. https://doi.org/10.1007/s00429-016-1228-7
Nieuwenhuys R, Puelles L (2016) Towards a new neuromorphology. Springer, Berlin
Nimchinsky EA, Hof PR, Young WG, Morrison JH (1996) Neurochemical, morphologic, and laminar characterization of cortical projection neurons in the cingulate motor areas of the macaque monkey. J Comp Neurol 374:136–160
Noctor SC, Martinez-Cerdeno V, Kriegstein AR (2007) Contribution of intermediate progenitor cells to cortical histogenesis. Arch Neurol 64(5):639–642. https://doi.org/10.1001/archneur.64.5.639
Nowakowski TJ, Bhaduri A, Pollen AA, Alvarado B, Mostajo-Radji MA, Di Lullo E, Haeussler M, Sandoval-Espinosa C, Liu SJ, Velmeshev D, Ounadjela JR, Shuga J, Wang X, Lim DA, West JA, Leyrat AA, Kent WJ, Kriegstein AR (2017) Spatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex. Science 358(6368):1318–1323. https://doi.org/10.1126/science.aap8809
Palomero-Gallagher N, Zilles K (2017) Cortical layers: Cyto-, myelo-, receptor- and synaptic architecture in human cortical areas. Neuroimage. https://doi.org/10.1016/j.neuroimage.2017.08.035
Palomero-Gallagher N, Zilles K (2018) Cyto- and receptor architectonic mapping of the human brain. Handb Clin Neurol 150:355–387. https://doi.org/10.1016/B978-0-444-63639-3.00024-4
Palomero-Gallagher N, Mohlberg H, Zilles K, Vogt B (2008) Cytology and receptor architecture of human anterior cingulate cortex. J Comp Neurol 508(6):906–926. https://doi.org/10.1002/cne.21684
Palomero-Gallagher N, Vogt BA, Schleicher A, Mayberg HS, Zilles K (2009) Receptor architecture of human cingulate cortex: evaluation of the four-region neurobiological model. Hum Brain Mapp 30(8):2336–2355. https://doi.org/10.1002/hbm.20667
Palomero-Gallagher N, Hoffstaedter F, Mohlberg H, Eickhoff SB, Amunts K, Zilles K (2018) Human pregenual anterior cingulate cortex: structural, functional, and connectional heterogeneity. Cereb Cortex. https://doi.org/10.1093/cercor/bhy124
Pandya DN, Sanides F (1973) Architectonic parcellation of the temporal operculum in rhesus monkey and its projection pattern. ZAnatEntwickl-Gesch 139:127–161
Pandya DN, Barbas H, Golberg G (1985) Architecture and connections of the premotor areas in the rhesus monkey [Commentary to Supplementary motor area structure and function: Review and hypotheses, Golberg G (1985); Behav Brain Sci, 8: 567-616]. Behav Brain Sci 8:595–596
Pandya DN, Seltzer B, Barbas H (1988) Input-output organization of the primate cerebral cortex. In: Steklis HD, Erwin J (eds) Comparative primate biology, vol 4. Neurosciences, Alan R. Liss, New York (NY), pp 39–80
Pandya D, Seltzer B, Petrides M, Cipolloni PB (2015) Cerebral cortex: architecture, connections, and the dual origin concept. Oxford University Press, New York
Penfield W, Jasper H (1954) Epilepsy and the functional anatomy of the human brain. Little, Brown and Company, Boston
Petrides M, Tomaiuolo F, Yeterian EH, Pandya DN (2012) The prefrontal cortex: comparative architectonic organization in the human and the macaque monkey brains. Cortex 48(1):46–57. https://doi.org/10.1016/j.cortex.2011.07.002
Popper KR (1959) The logic of scientific discovery. Basic Books, New York
Puelles L (2011) Pallio-pallial tangential migrations and growth signaling: new scenario for cortical evolution? Brain behavior evolution 78(1):108–127. https://doi.org/10.1159/000327905
Puelles L (2017) Comments on the updated tetrapartite pallium model in the mouse and chick, featuring a homologous claustro-insular complex. Brain Behav Evol 90(2):171–189. https://doi.org/10.1159/000479782
Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425–426
Rakic P (1976a) Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature 261:467–471
Rakic P (1976b) Differences in the time of origin and in eventual distribution of neurons in areas 17 and 18 of visual cortex in rhesus monkey. Exp Brain Res Suppl 1:244–248
Rakic P (2002) Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat Rev Neurosci 3(1):65–71
Ramón y Cajal S (1904/2002) Textura del sistema nervioso del hombre y de los vertebrados. Tomo II, segunda parte. Gobierno de Aragón. Departamento de Cultura y Turismo, Zaragoza
Ramón y Cajal S (1937) Recollections of my life. Memoirs of the American philosophical society, vol VIII, pt I-II, 1937. The American philosophical society, Philadelphia
Reep R (1984) Relationship between prefrontal and limbic cortex: a comparative and anatomical review. Brain Behav Evol 25:1–80
Reillo I, Romero CD, García-Cabezas MA, Borrell V (2011) A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb Cortex 21(7):1674–1694
Rempel-Clower NL, Barbas H (2000) The laminar pattern of connections between prefrontal and anterior temporal cortices in the rhesus monkey is related to cortical structure and function. Cereb Cortex 10(9):851–865
Rockland KS, Pandya DN (1979) Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res 179:3–20
Romanski LM, Tian B, Fritz J, Mishkin M, Goldman-Rakic PS, Rauschecker JP (1999) Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci 2:1131–1136
Rosa MG, Casagrande VA, Preuss T, Kaas JH (1997) Visual field representation in striate and prestriate cortices of a prosimian primate (Galago garnetti). J Neurophysiol 77:3193–3217
Roy M, Sorokina O, Skene N, Simonnet C, Mazzo F, Zwart R, Sher E, Smith C, Armstrong JD, Grant SGN (2018) Proteomic analysis of postsynaptic proteins in regions of the human neocortex. Nat Neurosci 21(1):130–138. https://doi.org/10.1038/s41593-017-0025-9
Sanides F (1962) Architectonics of the human frontal lobe of the brain. With a demonstration of the principles of its formation as a reflection of phylogenetic differentiation of the cerebral cortex. Monographien aus dem Gesamtgebiete der Neurologie Psychiatrie 98:1–201
Sanides F (1964) The cyto-myeloarchitecture of the human frontal lobe and its relation to phylogenetic differentiation of the cerebral cortex. J Hirnforsch 7:269–282
Sanides F (1968) The architecture of the cortical taste nerve areas in squirrel monkey (Saimiri sciureus) and their relationships to insular, sensorimotor and prefrontal regions. Brain Res 8:97–124
Sanides F (1970) Functional architecture of motor and sensory cortices in primates in the light of a new concept of neocortex evolution. In: Noback CR, Montagna W (eds) The primate brain: advances in primatology. Appleton-Century-Crofts Educational Division/Meredith Corporation, New York (NY), pp 137–208
Sanides F (1972) Representation in the cerebral cortex and its areal lamination pattern. In: Bourne GH (ed) the structure and function of nervous tissue, vol V. Academic Press, New York & London, pp 329–453
Sanides F, Hoffmann J (1969) Cyto- and myeloarchitecture of the visual cortex of the cat and of the surrounding integration cortices. J Hirnforsch 11(1):79–104
Sanides F, Krishnamurti A (1967) Cytoarchitectonic subdivisions of sensorimotor and prefrontal regions and of bordering insular and limbic fields in slow loris (Nycticebus coucang coucang). J Hirnforsch 9:225–252
Santos M, Uppal N, Butti C, Wicinski B, Schmeidler J, Giannakopoulos P, Heinsen H, Schmitz C, Hof PR (2011) Von Economo neurons in autism: a stereologic study of the frontoinsular cortex in children. Brain Res 1380:206–217. https://doi.org/10.1016/j.brainres.2010.08.067
Scholtens LH, van den Heuvel MP (2018) Multimodal connectomics in psychiatry: bridging scales from micro to macro. Biol Psychiatry Cognit Neurosci Neuroimaging. https://doi.org/10.1016/j.bpsc.2018.03.017
Scholtens LH, Feldman Barrett L, van den Heuvel MP (2018) Cross-species evidence of interplay between neural connectivity at the micro- and macroscale of connectome organization in human, mouse, and rat brain. Brain Connect 8(10):595–603. https://doi.org/10.1089/brain.2018.0622
Sidman RL, Rakic P (1973) Neuronal migration, with special reference to developing human brain: a review. Brain Res 62:1–35
Siegel RL, Miller KD, Jemal A (2018) Cancer statistics, 2018. CA Cancer J Clin 68(1):7–30. https://doi.org/10.3322/caac.21442
Smart IH, Dehay C, Giroud P, Berland M, Kennedy H (2002) Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 12(1):37–53
Subramanian L, Remedios R, Shetty A, Tole S (2009) Signals from the edges: the cortical hem and antihem in telencephalic development. Semin Cell Dev Biol 20(6):712–718. https://doi.org/10.1016/j.semcdb.2009.04.001
Tucker DM, Brown M, Luu P, Holmes MD (2007) Discharges in ventromedial frontal cortex during absence spells. E&B 11(4):546–557
Ungerleider L, Mishkin M (1982) Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT Press, Cambridge, pp 549–586
van Kooten IA, Palmen SJ, von Cappeln P, Steinbusch HW, Korr H, Heinsen H, Hof PR, van Engeland H, Schmitz C (2008) Neurons in the fusiform gyrus are fewer and smaller in autism. Brain 131(Pt 4):987–999
van den Heuvel MP, Yeo BTT (2017) A spotlight on bridging microscale and macroscale human brain architecture. Neuron 93(6):1248–1251. https://doi.org/10.1016/j.neuron.2017.02.048
van den Heuvel MP, Scholtens LH, Feldman Barrett L, Hilgetag CC, de Reus MA (2015) Bridging cytoarchitectonics and connectomics in human cerebral cortex. J Neurosci 35(41):13943–13948. https://doi.org/10.1523/JNEUROSCI.2630-15.2015
Vogt C, Vogt O (1919) Allgemeinere Ergebnisse unserer Hirnforschung. J Psychol Neurol 25:279–462
von Economo C (1927/2009) Cellular structure of the human cerebral cortex (Translated and edited by Lazaros C. Triarhou). Karger, Basel (Switzerland)
Wagner GP (1989) The origin of morphological characters and the biological basis of homology. Evol Int J Organ Evol 43(6):1157–1171. https://doi.org/10.1111/j.1558-5646.1989.tb02566.x
Wegiel J, Kuchna I, Nowicki K, Imaki H, Marchi E, Ma SY, Chauhan A, Chauhan V, Bobrowicz TW, de Leon M, Louis LA, Cohen IL, London E, Brown WT, Wisniewski T (2010) The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol 119(6):755–770
Wei Y, Scholtens LH, Turk E, Van den Heuvel MP (2019) Multiscale examination of cytoarchitectonic similarity and human brain connectivity. Netw Neurosci 3(1):124–137. https://doi.org/10.1162/netn_a_00057
Weinberg RA (2014) Coming full circle-from endless complexity to simplicity and back again. Cell 157(1):267–271. https://doi.org/10.1016/j.cell.2014.03.004
Wise SP (2008) Forward frontal fields: phylogeny and fundamental function. Trends Neurosci 31(12):599–608. https://doi.org/10.1016/j.tins.2008.08.008
Woodworth MB, Girskis KM, Walsh CA (2017) Building a lineage from single cells: genetic techniques for cell lineage tracking. Nat Rev Genet 18(4):230–244. https://doi.org/10.1038/nrg.2016.159
Woolsey CN (1963) Comparative studies on localization in precentral and supplementary motor areas. Int J Neurol 4:13–20
Yakovlev PI (1959) Pathoarchitectonic studies of cerebral malformations. III. Arrhinencephalies (holotelencephalies). J Neuropathol Exp Neurol 18(1):22–55
Zikopoulos B, Barbas H (2010) Changes in prefrontal axons may disrupt the network in autism. J Neurosci 30(44):14595–14609
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
Zikopoulos B, Garcia-Cabezas MA, Barbas H (2018a) Parallel trends in cortical grey and white matter architecture and connections in primates allow fine study of pathways in humans and reveal network disruptions in autism. PLoS Biol. https://doi.org/10.1371/journal.pbio.2004559
Zikopoulos B, Liu X, Tepe J, Trutzer I, John YJ, Barbas H (2018b) Opposite development of short- and long-range anterior cingulate pathways in autism. Acta Neuropathol. https://doi.org/10.1007/s00401-018-1904-1
Zilles KJ (1985) The cortex of the rat: a stereotaxic atlas. Springer, Berlin
Zilles K, Palomero-Gallagher N (2017) Multiple transmitter receptors in regions and layers of the human cerebral cortex. Front Neuroanat 11:78. https://doi.org/10.3389/fnana.2017.00078
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García-Cabezas, M.Á., Zikopoulos, B. & Barbas, H. The Structural Model: a theory linking connections, plasticity, pathology, development and evolution of the cerebral cortex. Brain Struct Funct 224, 985–1008 (2019). https://doi.org/10.1007/s00429-019-01841-9
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DOI: https://doi.org/10.1007/s00429-019-01841-9