Abstract
Synaptic transmission between neurons is the basic unit of communication in neural circuits. The relative number and distribution of excitatory and inhibitory synaptic inputs across individual dendrites and neurons are the hardware of local dendritic and cellular computations. In this chapter, we discuss the structural and functional observations that have guided the understanding of excitatory and inhibitory synaptic organization across the neuronal arbor, the subcellular targeting properties of different neuronal subtypes, and the effects of synaptic placement on local integration within dendritic segments. We focus primarily on the adult mammalian cortex and hippocampus, where excitatory and inhibitory cell types, their connectivity, and its functional implications have been best characterized.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Aoki C, Miko I, Oviedo H, Mikeladze-Dvali T, Alexandre L, Sweeney N, Bredt DS (2001) Electron microscopic immunocytochemical detection of PSD-95, PSD-93, SAP-102, and SAP-97 at postsynaptic, presynaptic, and nonsynaptic sites of adult and neonatal rat visual cortex. Synapse 40:239–257
Arellano JI, Espinosa A, Fairen A, Yuste R, DeFelipe J (2007) Non-synaptic dendritic spines in neocortex. Neuroscience 145:464–469
Avermann M, Tomm C, Mateo C, Gerstner W, Petersen CC (2012) Microcircuits of excitatory and inhibitory neurons in layer 2/3 of mouse barrel cortex. J Neurophysiol 107:3116–3134
Azouz R, Gray CM, Nowak LG, McCormick DA (1997) Physiological properties of inhibitory interneurons in cat striate cortex. Cereb Cortex 7:534–545
Bar-Ilan L, Gidon A, Segev I (2012) The role of dendritic inhibition in shaping the plasticity of excitatory synapses. Front Neural Circ 6:118
Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA, Somogyi P (1993) The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771–787
Belgard TG, Marques AC, Oliver PL, Abaan HO, Sirey TM, Hoerder-Suabedissen A, Garcia-Moreno F, Molnar Z, Margulies EH, Ponting CP (2011) A transcriptomic atlas of mouse neocortical layers. Neuron 71:605–616
Benshalom G, White EL (1986) Quantification of thalamocortical synapses with spiny stellate neurons in layer IV of mouse somatosensory cortex. J Comp Neurol 253:303–314
Bi G, Poo M (2001) Synaptic modification by correlated activity: Hebb’s postulate revisited. Ann Rev Neurosci 24:139–166
Branco T, Clark BA, Hausser M (2010) Dendritic discrimination of temporal input sequences in cortical neurons. Science 329:1671–1675
Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823–828
Cane M, Maco B, Knott G, Holtmaat A (2014) The relationship between PSD-95 clustering and spine stability in vivo. J Neurosci 34:2075–2086
Chadderton P, Schaefer AT, Williams SR, Margrie TW (2014) Sensory-evoked synaptic integration in cerebellar and cerebral cortical neurons. Nat Rev Neurosci 15:71–83
Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24:9598–9611
Chen JL, Flanders GH, Lee WC, Lin WC, Nedivi E (2011a) Inhibitory dendrite dynamics as a general feature of the adult cortical microcircuit. J Neurosci 31:12437–12443
Chen JL, Lin WC, Cha JW, So PT, Kubota Y, Nedivi E (2011b) Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat Neurosci 14:587–U573
Chen X, Leischner U, Rochefort NL, Nelken I, Konnerth A (2011c) Functional mapping of single spines in cortical neurons in vivo. Nature 475:501–505
Chen JL, Villa KL, Cha JW, So PT, Kubota Y, Nedivi E (2012) Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron 74:361–373
Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V et al (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:295–300
Chiu CQ, Lur G, Morse TM, Carnevale NT, Ellis-Davies GC, Higley MJ (2013) Compartmentalization of GABAergic inhibition by dendritic spines. Science 340:759–762
Constantinople CM, Bruno RM (2013) Deep cortical layers are activated directly by thalamus. Science 340:1591–1594
Dani VS, Chang Q, Maffei A, Turrigiano GG, Jaenisch R, Nelson SB (2005) Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc Natl Acad Sci U S A 102:12560–12565
Davis TL, Sterling P (1979) Microcircuitry of cat visual cortex: classification of neurons in layer IV of area 17, and identification of the patterns of lateral geniculate input. J Comp Neurol 188:599–627
DeBello WM, McBride TJ, Nichols GS, Pannoni KE, Sanculi D, Totten DJ (2014) Input clustering and the microscale structure of local circuits. Front Neural Circ 8:112
DeFelipe J, Lopez-Cruz PL, Benavides-Piccione R, Bielza C, Larranaga P, Anderson S, Burkhalter A, Cauli B, Fairen A, Feldmeyer D et al (2013) New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat Rev Neurosci 14:202–216
Di Cristo G, Wu C, Chattopadhyaya B, Ango F, Knott G, Welker E, Svoboda K, Huang ZJ (2004) Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs. Nat Neurosci 7:1184–1186
Druckmann S, Feng L, Lee B, Yook C, Zhao T, Magee JC, Kim J (2014) Structured synaptic connectivity between hippocampal regions. Neuron 81:629–640
Elias GM, Elias LA, Apostolides PF, Kriegstein AR, Nicoll RA (2008) Differential trafficking of AMPA and NMDA receptors by SAP102 and PSD-95 underlies synapse development. Proc Natl Acad Sci U S A 105:20953–20958
Elston GN, Rosa MG (1997) The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cereb Cortex 7:432–452
Fanselow EE, Richardson KA, Connors BW (2008) Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 100:2640–2652
Feldman ML, Peters A (1978) The forms of non-pyramidal neurons in the visual cortex of the rat. J Comp Neurol 179:761–793
Feldmeyer D (2012) Excitatory neuronal connectivity in the barrel cortex. Front Neuroanat 6:24
Feldmeyer D, Lubke J, Silver RA, Sakmann B (2002) Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J Geophys Res 538:803–822
Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47
Fifkova E, Eason H, Schaner P (1992) Inhibitory contacts on dendritic spines of the dentate fascia. Brain Res 577:331–336
Fino E, Yuste R (2011) Dense inhibitory connectivity in neocortex. Neuron 69:1188–1203
Gabbott PL, Somogyi P (1986) Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat. Exp Brain Res 61:323–331
Gambino F, Pages S, Kehayas V, Baptista D, Tatti R, Carleton A, Holtmaat A (2014) Sensory-evoked LTP driven by dendritic plateau potentials in vivo. Nature 515:116–119
Gasparini S, Magee JC (2006) State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J Neurosci 26:2088–2100
Gerfen CR, Paletzki R, Heintz N (2013) GENSAT BAC cre-recombinase driver lines to study the functional organization of cerebral cortical and basal ganglia circuits. Neuron 80:1368–1383
Gidon A, Segev I (2012) Principles governing the operation of synaptic inhibition in dendrites. Neuron 75:330–341
Golding NL, Spruston N (1998) Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21:1189–1200
Golding NL, Kath WL, Spruston N (2001) Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. J Neurophysiol 86:2998–3010
Golding NL, Staff NP, Spruston N (2002) Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418:326–331
Golding NL, Mickus TJ, Katz Y, Kath WL, Spruston N (2005) Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites. J Geophys Res 568:69–82
Gong S, Doughty M, Harbaugh CR, Cummins A, Hatten ME, Heintz N, Gerfen CR (2007) Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J Neurosci 27:9817–9823
Gordon U, Polsky A, Schiller J (2006) Plasticity compartments in basal dendrites of neocortical pyramidal neurons. J Neurosci 26:12717–12726
Grienberger C, Chen X, Konnerth A (2014) NMDA receptor-dependent multidendrite Ca(2+) spikes required for hippocampal burst firing in vivo. Neuron 81:1274–1281
Grienberger C, Chen X, Konnerth A (2015) Dendritic function in vivo. Trends Neurosci 38:45–54
Grutzendler J, Kasthuri N, Gan WB (2002) Long-term dendritic spine stability in the adult cortex. Nature 420:812–816
Gulyas AI, Miettinen R, Jacobowitz DM, Freund TF (1992) Calretinin is present in non-pyramidal cells of the rat hippocampus--I. A new type of neuron specifically associated with the mossy fibre system. Neuroscience 48:1–27
Gulyas AI, Megias M, Emri Z, Freund TF (1999) Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J Neurosci 19:10082–10097
Hao J, Wang XD, Dan Y, Poo MM, Zhang XH (2009) An arithmetic rule for spatial summation of excitatory and inhibitory inputs in pyramidal neurons. Proc Natl Acad Sci U S A 106:21906–21911
Harauzov A, Spolidoro M, DiCristo G, De Pasquale R, Cancedda L, Pizzorusso T, Viegi A, Berardi N, Maffei L (2010) Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J Neurosci 30:361–371
Harris KM, Jensen FE, Tsao B (1992) Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 12:2685–2705
Hayama T, Noguchi J, Watanabe S, Takahashi N, Hayashi-Takagi A, Ellis-Davies GC, Matsuzaki M, Kasai H (2013) GABA promotes the competitive selection of dendritic spines by controlling local Ca2+ signaling. Nat Neurosci 16:1409–1416
Hersch SM, White EL (1981) Quantification of synapses formed with apical dendrites of Golgi-impregnated pyramidal cells: variability in thalamocortical inputs, but consistency in the ratios of asymmetrical to symmetrical synapses. Neuroscience 6:1043–1051
Higley MJ (2014) Localized GABAergic inhibition of dendritic Ca(2+) signalling. Nat Rev Neurosci 15:567–572
Higley MJ, Contreras D (2006) Balanced excitation and inhibition determine spike timing during frequency adaptation. J Neurosci 26:448–457
Hioki H, Okamoto S, Konno M, Kameda H, Sohn J, Kuramoto E, Fujiyama F, Kaneko T (2013) Cell type-specific inhibitory inputs to dendritic and somatic compartments of parvalbumin-expressing neocortical interneuron. J Neurosci 33:544–555
Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M (2009) Experience leaves a lasting structural trace in cortical circuits. Nature 457:313–317
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
Huang ZJ (2014) Toward a genetic dissection of cortical circuits in the mouse. Neuron 83:1284–1302
Isshiki M, Tanaka S, Kuriu T, Tabuchi K, Takumi T, Okabe S (2014) Enhanced synapse remodelling as a common phenotype in mouse models of autism. Nat Commun 5:4742
Jia H, Rochefort NL, Chen X, Konnerth A (2010) Dendritic organization of sensory input to cortical neurons in vivo. Nature 464:1307–1312
Jiang X, Wang G, Lee AJ, Stornetta RL, Zhu JJ (2013) The organization of two new cortical interneuronal circuits. Nat Neurosci 16:210–218
Karube F, Kubota Y, Kawaguchi Y (2004) Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes. J Neurosci 24:2853–2865
Kawaguchi Y (1997) Selective cholinergic modulation of cortical GABAergic cell subtypes. J Neurophysiol 78:1743–1747
Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476–486
Kawaguchi Y, Kubota Y (1998) Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85:677–701
Kawaguchi Y, Karube F, Kubota Y (2006) Dendritic branch typing and spine expression patterns in cortical nonpyramidal cells. Cereb Cortex 16:696–711
Keck T, Mrsic-Flogel TD, Vaz Afonso M, Eysel UT, Bonhoeffer T, Hubener M (2008) Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nat Neurosci 11:1162–1167
Keck T, Scheuss V, Jacobsen RI, Wierenga CJ, Eysel UT, Bonhoeffer T, Hubener M (2011) Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 71:869–882
Khirug S, Yamada J, Afzalov R, Voipio J, Khiroug L, Kaila K (2008) GABAergic depolarization of the axon initial segment in cortical principal neurons is caused by the Na-K-2Cl cotransporter NKCC1. J Neurosci 28:4635–4639
Kim HG, Beierlein M, Connors BW (1995) Inhibitory control of excitable dendrites in neocortex. J Neurophysiol 74:1810–1814
Kisvarday ZF, Martin KA, Whitteridge D, Somogyi P (1985) Synaptic connections of intracellularly filled clutch cells: a type of small basket cell in the visual cortex of the cat. J Comp Neurol 241:111–137
Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53–57
Kleindienst T, Winnubst J, Roth-Alpermann C, Bonhoeffer T, Lohmann C (2011) Activity-dependent clustering of functional synaptic inputs on developing hippocampal dendrites. Neuron 72:1012–1024
Kleschevnikov AM, Belichenko PV, Villar AJ, Epstein CJ, Malenka RC, Mobley WC (2004) Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of down syndrome. J Neurosci 24:8153–8160
Knott GW, Quairiaux C, Genoud C, Welker E (2002) Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34:265–273
Kubota Y (2014) Untangling GABAergic wiring in the cortical microcircuit. Curr Opinion Neurobiol 26:7–14
Kubota Y, Hattori R, Yui Y (1994) Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res 649:159–173
Kubota Y, Hatada S, Kondo S, Karube F, Kawaguchi Y (2007) Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents. J Neurosci 27:1139–1150
Kubota Y, Shigematsu N, Karube F, Sekigawa A, Kato S, Yamaguchi N, Hirai Y, Morishima M, Kawaguchi Y (2011) Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons. Cereb Cortex 21:1803–1817
Larkman AU (1991) Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions. J Comp Neurol 306:332–343
Larkum M (2013) A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex. Trends Neurosci 36:141–151
Larkum ME, Zhu JJ, Sakmann B (1999) A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398:338–341
Larkum ME, Nevian T, Sandler M, Polsky A, Schiller J (2009) Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 325:756–760
Larsen DD, Callaway EM (2006) Development of layer-specific axonal arborizations in mouse primary somatosensory cortex. J Comp Neurol 494:398–414
Lee WC, Huang H, Feng G, Sanes JR, Brown EN, So PT, Nedivi E (2006) Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biol 4, e29
Lee WC, Chen JL, Huang H, Leslie JH, Amitai Y, So PT, Nedivi E (2008) A dynamic zone defines interneuron remodeling in the adult neocortex. Proc Natl Acad Sci U S A 105:19968–19973
Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B (2010) The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci 30:16796–16808
Lee S, Kruglikov I, Huang ZJ, Fishell G, Rudy B (2013) A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat Neurosci 16:1662–1670
Lefort S, Tomm C, Floyd Sarria JC, Petersen CC (2009) The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 61:301–316
LeVay S (1973) Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi preparations. J Comp Neurol 150:53–85
Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312–324
Li XG, Somogyi P, Ylinen A, Buzsaki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181–208
Li S, Liu N, Zhang XH, Zhou D, Cai D (2014) Bilinearity in spatiotemporal integration of synaptic inputs. PLoS Comp Biol 10, e1004014
Major G, Larkum ME, Schiller J (2013) Active properties of neocortical pyramidal neuron dendrites. Ann Rev Neurosci 36:1–24
Makino H, Malinow R (2011) Compartmentalized versus global synaptic plasticity on dendrites controlled by experience. Neuron 72:1001–1011
Maya Vetencourt JF, Sale A, Viegi A, Baroncelli L, De Pasquale R, O’Leary OF, Castren E, Maffei L (2008) The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 320:385–388
McBride TJ, Rodriguez-Contreras A, Trinh A, Bailey R, Debello WM (2008) Learning drives differential clustering of axodendritic contacts in the barn owl auditory system. J Neurosci 28:6960–6973
Megias M, Emri Z, Freund TF, Gulyas AI (2001) Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527–540
Mel BW (1993) Synaptic integration in an excitable dendritic tree. J Neurophysiol 70:1086–1101
Miles R, Toth K, Gulyas AI, Hajos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815–823
Mizrahi A, Katz LC (2003) Dendritic stability in the adult olfactory bulb. Nat Neurosci 6:1201–1207
Mohler H, Fritschy JM, Crestani F, Hensch T, Rudolph U (2004) Specific GABA(A) circuits in brain development and therapy. Biochem Pharmacol 68:1685–1690
Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8:427–437
Morishima M, Morita K, Kubota Y, Kawaguchi Y (2011) Highly differentiated projection-specific cortical subnetworks. J Neurosci 31:10380–10391
Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW (2000) Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20:3354–3368
Palmer LM (2014) Dendritic integration in pyramidal neurons during network activity and disease. Brain Res Bull 103:2–10
Parnavelas JG, Sullivan K, Lieberman AR, Webster KE (1977) Neurons and their synaptic organization in the visual cortex of the rat. Electron microscopy of Golgi preparations. Cell Tissue Res 183:499–517
Perez-Garci E, Gassmann M, Bettler B, Larkum ME (2006) The GABAB1b isoform mediates long-lasting inhibition of dendritic Ca2+ spikes in layer 5 somatosensory pyramidal neurons. Neuron 50:603–616
Peters A, Payne BR (1993) Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb Cortex 3:69–78
Petilla Interneuron Nomenclature G, Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J et al (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557–568
Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M (2013) Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci 16:1068–1076
Pi HJ, Hangya B, Kvitsiani D, Sanders JI, Huang ZJ, Kepecs A (2013) Cortical interneurons that specialize in disinhibitory control. Nature 503:521–524
Pieraut S, Gounko N, Sando R 3rd, Dang W, Rebboah E, Panda S, Madisen L, Zeng H, Maximov A (2014) Experience-dependent remodeling of basket cell networks in the dentate gyrus. Neuron 84:107–122
Pouille F, Scanziani M (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159–1163
Rubenstein JL, Merzenich MM (2003) Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2:255–267
Rudy B, Fishell G, Lee S, Hjerling-Leffler J (2011) Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 71:45–61
Sans N, Petralia RS, Wang YX, Blahos J 2nd, Hell JW, Wenthold RJ (2000) A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J Neurosci 20:1260–1271
Schoonover CE, Tapia JC, Schilling VC, Wimmer V, Blazeski R, Zhang W, Mason CA, Bruno RM (2014) Comparative strength and dendritic organization of thalamocortical and corticocortical synapses onto excitatory layer 4 neurons. J Neurosci 34:6746–6758
Schubert D, Staiger JF, Cho N, Kotter R, Zilles K, Luhmann HJ (2001) Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J Neurosci 21:3580–3592
Schuemann A, Klawiter A, Bonhoeffer T, Wierenga CJ (2013) Structural plasticity of GABAergic axons is regulated by network activity and GABAA receptor activation. Front Neural Circ 7:113
Silver RA, Lubke J, Sakmann B, Feldmeyer D (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302:1981–1984
Sivyer B, Williams SR (2013) Direction selectivity is computed by active dendritic integration in retinal ganglion cells. Nat Neurosci 16:1848–1856
Somogyi P (1977) A specific ‘axo-axonal’ interneuron in the visual cortex of the rat. Brain Res 136:345–350
Somogyi P, Freund TF, Cowey A (1982) The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey. Neuroscience 7:2577–2607
Song S, Miller KD, Abbott LF (2000) Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci 3:919–926
Sorensen SA, Bernard A, Menon V, Royall JJ, Glattfelder KJ, Desta T, Hirokawa K, Mortrud M, Miller JA, Zeng H et al (2015) Correlated gene expression and target specificity demonstrate excitatory projection neuron diversity. Cereb Cortex 25:433–449
Spruston N (2008) Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9:206–221
Stokes CC, Teeter CM, Isaacson JS (2014) Single dendrite-targeting interneurons generate branch-specific inhibition. Front Neural Circ 8:139
Szabadics J, Varga C, Molnar G, Olah S, Barzo P, Tamas G (2006) Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311:233–235
Takahashi N, Kitamura K, Matsuo N, Mayford M, Kano M, Matsuki N, Ikegaya Y (2012) Locally synchronized synaptic inputs. Science 335:353–356
Taniguchi H, Lu J, Huang ZJ (2013) The spatial and temporal origin of chandelier cells in mouse neocortex. Science 339:70–74
Thomson AM, Deuchars J (1997) Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb Cortex 7:510–522
Thomson AM, Lamy C (2007) Functional maps of neocortical local circuitry. Front Neurosci 1:19–42
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
Trommald M, Jensen V, Andersen P (1995) Analysis of dendritic spines in rat CA1 pyramidal cells intracellularly filled with a fluorescent dye. J Comp Neurol 353:260–274
Uematsu M, Hirai Y, Karube F, Ebihara S, Kato M, Abe K, Obata K, Yoshida S, Hirabayashi M, Yanagawa Y et al (2008) Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex 18:315–330
van Versendaal D, Rajendran R, Saiepour MH, Klooster J, Smit-Rigter L, Sommeijer JP, De Zeeuw CI, Hofer SB, Heimel JA, Levelt CN (2012) Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron 74:374–383
Varga Z, Jia H, Sakmann B, Konnerth A (2011) Dendritic coding of multiple sensory inputs in single cortical neurons in vivo. Proc Natl Acad Sci U S A 108:15420–15425
Villa KL, Berry KP, Subramanian J, Cha JW, Oh WC, Kwon HB, Kubota Y, So PT, Nedivi E (2016) Inhibitory synapses are repeatedly assembled and removed at persistent sites in vivo. Neuron 89:756–769
Westrum LE (1966) Synaptic contacts on axons in the cerebral cortex. Nature 210:1289–1290
White EL, Rock MP (1980) Three-dimensional aspects and synaptic relationships of a Golgi-impregnated spiny stellate cell reconstructed from serial thin sections. J Neurocytol 9:615–636
Wierenga CJ, Becker N, Bonhoeffer T (2008) GABAergic synapses are formed without the involvement of dendritic protrusions. Nat Neurosci 11:1044–1052
Willadt S, Nenniger M, Vogt KE (2013) Hippocampal feedforward inhibition focuses excitatory synaptic signals into distinct dendritic compartments. PLoS One 8, e80984
Winnubst J, Lohmann C (2012) Synaptic clustering during development and learning: the why, when, and how. Front Mol Neurosci 5:70
Woodruff A, Xu Q, Anderson SA, Yuste R (2009) Depolarizing effect of neocortical chandelier neurons. Front Neural Circ 3:15
Woodruff AR, Anderson SA, Yuste R (2010) The enigmatic function of chandelier cells. Front Neurosci 4:201
Woodruff AR, McGarry LM, Vogels TP, Inan M, Anderson SA, Yuste R (2011) State-dependent function of neocortical chandelier cells. J Neurosci 31:17872–17886
Xu H, Jeong HY, Tremblay R, Rudy B (2013) Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 77:155–167
Zhang D, Li Y, Rasch MJ, Wu S (2013) Nonlinear multiplicative dendritic integration in neuron and network models. Front Comp Neurosci 7:56
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer Japan
About this chapter
Cite this chapter
Villa, K.L., Nedivi, E. (2016). Excitatory and Inhibitory Synaptic Placement and Functional Implications. In: Emoto, K., Wong, R., Huang, E., Hoogenraad, C. (eds) Dendrites. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56050-0_18
Download citation
DOI: https://doi.org/10.1007/978-4-431-56050-0_18
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-56048-7
Online ISBN: 978-4-431-56050-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)