Neuronal activity controls the development of interneurons in the somatosensory cortex

Abstract

BACKGROUND: Neuronal activity in cortical areas regulates neurodevelopment by interacting with defined genetic programs to shape the mature central nervous system. Electrical activity is conveyed to sensory cortical areas via intracortical and thalamocortical neurons, and includes oscillatory patterns that have been measured across cortical regions.

OBJECTIVE: In this work, we review the most recent findings about how electrical activity shapes the developmental assembly of functional circuitry in the somatosensory cortex, with an emphasis on interneuron maturation and integration. We include studies on the effect of various neurotransmitters and on the influence of thalamocortical afferent activity on circuit development. We additionally reviewed studies describing network activity patterns.

METHODS: We conducted an extensive literature search using both the PubMed and Google Scholar search engines. The following keywords were used in various iterations: “interneuron”, “somatosensory”, “development”, “activity”, “network patterns”, “thalamocortical”, “NMDA receptor”, “plasticity”. We additionally selected papers known to us from past reading, and those recommended to us by reviewers and members of our lab.

RESULTS: We reviewed a total of 132 articles that focused on the role of activity in interneuronal migration, maturation, and circuit development, as well as the source of electrical inputs and patterns of cortical activity in the somatosensory cortex. 79 of these papers included in this timely review were written between 2007 and 2016.

CONCLUSIONS: Neuronal activity shapes the developmental assembly of functional circuitry in the somatosensory cortical interneurons. This activity impacts nearly every aspect of development and acquisition of mature neuronal characteristics, and may contribute to changing phenotypes, altered transmitter expression, and plasticity in the adult. Progressively changing oscillatory network patterns contribute to this activity in the early postnatal period, although a direct requirement for specific patterns and origins of activity remains to be demonstrated.

Keywords

interneuron / neurodevelopment / neuroplasticity / thalamocortical / NMDA receptors / neuronal maturation

References

[1] Adelsberger H, Garaschuk O, Konnerth A (2005). Cortical calcium waves in resting newborn mice. Nat Neurosci, 8(8): 988–990

[2] Agmon A, Connors B W (1992). Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci, 12(1): 319–329

[3] Agmon A, O’Dowd D K (1992). NMDA receptor-mediated currents are prominent in the thalamocortical synaptic response before maturation of inhibition. J Neurophysiol, 68(1): 345–349

[4] Allène C, Cattani A, Ackman J B, Bonifazi P, Aniksztejn L, Ben-Ari Y, Cossart R (2008). Sequential generation of two distinct synapse-driven network patterns in developing neocortex. J Neurosci, 28(48): 12851–12863

[5] Allene C, Cossart R (2010). Early NMDA receptor-driven waves of activity in the developing neocortex: physiological or pathological network oscillations? J Physiol, 588(Pt 1): 83–91

[6] An S, Kilb W, Luhmann H J (2014). Sensory-evoked and spontaneous gamma and spindle bursts in neonatal rat motor cortex. J Neurosci, 34(33): 10870–10883

[7] Anastasiades P G, Marques-Smith A, Lyngholm D, Lickiss T, Raffiq S, Kätzel D, Miesenböck G, Butt S J (2016). GABAergic interneurons form transient layer-specific circuits in early postnatal neocortex. Nat Commun, 7: 10584

[8] Arroyo D A, Feller M B (2016). Spatiotemporal Features of Retinal Waves Instruct the Wiring of the Visual Circuitry. Front Neural Circuits, 10: 54

[9] Ascoli G A, Alonso-Nanclares L, Anderson S A, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsáki G, Cauli B, Defelipe J, Fairén A, Feldmeyer D, Fishell G, Fregnac Y, Freund T F, Gardner D, Gardner E P, Goldberg J H, Helmstaedter M, Hestrin S, Karube F, Kisvárday Z F, Lambolez B, Lewis D A, Marin O, Markram H, Muñoz A, Packer A, Petersen C C, Rockland K S, Rossier J, Rudy B, Somogyi P, Staiger J F, Tamas G, Thomson A M, Toledo-Rodriguez M, Wang Y, West D C, Yuste R, Yuste R, and the Petilla Interneuron Nomenclature Group (2008). Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci, 9(7): 557–568

[10] Avila A, Vidal P M, Dear T N, Harvey R J, Rigo J M, Nguyen L (2013). Glycine receptor α2 subunit activation promotes cortical interneuron migration. Cell Reports, 4(4): 738–750

[11] Baho E, Di Cristo G (2012). Neural activity and neurotransmission regulate the maturation of the innervation field of cortical GABAergic interneurons in an age-dependent manner. J Neurosci, 32(3): 911–918

[12] Bando Y, Irie K, Shimomura T, Umeshima H, Kushida Y, Kengaku M, Fujiyoshi Y, Hirano T, Tagawa Y (2016). Control of spontaneous Ca²⁺ transients is critical for neuronal maturation in the developing neocortex. Cereb Cortex, 26(1): 106–117

[13] Batista-Brito R, Fishell G (2009). The developmental integration of cortical interneurons into a functional network. Curr Top Dev Biol, 87: 81–118

[14] Batista-Brito R, Machold R, Klein C, Fishell G (2008). Gene expression in cortical interneuron precursors is prescient of their mature function. Cereb Cortex, 18(10): 2306–2317

[15] Behar T N, Schaffner A E, Scott C A, Greene C L, Barker J L (2000). GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb Cortex, 10(9): 899–909

[16] Behar T N, Scott C A, Greene C L, Wen X, Smith S V, Maric D, Liu Q Y, Colton C A, Barker J L (1999). Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci, 19(11): 4449–4461

[17] Bony G, Szczurkowska J, Tamagno I, Shelly M, Contestabile A, Cancedda L (2013). Non-hyperpolarizing GABAB receptor activation regulates neuronal migration and neurite growth and specification by cAMP/LKB1. Nat Commun, 4: 1800

[18] Bortone D, Polleux F (2009). KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron, 62(1): 53–71

[19] Butt S J, Fuccillo M, Nery S, Noctor S, Kriegstein A, Corbin J G, Fishell G (2005). The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron, 48(4): 591–604

[20] Campanac E, Gasselin C, Baude A, Rama S, Ankri N, Debanne D (2013). Enhanced intrinsic excitability in basket cells maintains excitatory-inhibitory balance in hippocampal circuits. Neuron, 77(4): 712–722

[21] Chaudhury S, Sharma V, Kumar V, Nag T C, Wadhwa S (2016). Activity-dependent synaptic plasticity modulates the critical phase of brain development. Brain Dev, 38(4): 355–363

[22] Chu J, Anderson S A (2015). Development of cortical interneurons. Neuropsychopharmacology, 40(1): 16–23

[23] Close J, Xu H, De Marco García N, Batista-Brito R, Rossignol E, Rudy B, Fishell G (2012). Satb1 is an activity-modulated transcription factor required for the terminal differentiation and connectivity of medial ganglionic eminence-derived cortical interneurons. J Neurosci, 32(49): 17690–17705

[24] Cohen-Kashi Malina K, Mohar B, Rappaport A N, Lampl I (2016). Local and thalamic origins of correlated ongoing and sensory-evoked cortical activities. Nat Commun, 7: 12740

[25] Colonnese M T, Kaminska A, Minlebaev M, Milh M, Bloem B, Lescure S, Moriette G, Chiron C, Ben-Ari Y, Khazipov R (2010). A conserved switch in sensory processing prepares developing neocortex for vision. Neuron, 67(3): 480–498

[26] Conhaim J, Easton C R, Becker M I, Barahimi M, Cedarbaum E R, Moore J G, Mather L F, Dabagh S, Minter D J, Moen S P, Moody W J (2011). Developmental changes in propagation patterns and transmitter dependence of waves of spontaneous activity in the mouse cerebral cortex. J Physiol, 589(Pt 10): 2529–2541

[27] Corlew R, Bosma M M, Moody W J (2004). Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones. J Physiol, 560(Pt 2): 377–390

[28] Cossart R, Ikegaya Y, Yuste R (2005). Calcium imaging of cortical networks dynamics. Cell Calcium, 37(5): 451–457

[29] Coulter D A (2001). Epilepsy-associated plasticity in gamma-aminobutyric acid receptor expression, function, and inhibitory synaptic properties. Int Rev Neurobiol, 45: 237–252

[30] Crair M C, Malenka R C (1995). A critical period for long-term potentiation at thalamocortical synapses. Nature, 375(6529): 325–328

[31] Cruikshank S J, Urabe H, Nurmikko A V, Connors B W (2010). Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron, 65(2): 230–245

[32] Cuzon V C, Yeh P W, Cheng Q, Yeh H H (2006). Ambient GABA promotes cortical entry of tangentially migrating cells derived from the medial ganglionic eminence. Cereb Cortex, 16(10): 1377–1388

[33] Cuzon Carlson V C, Yeh H H (2011). GABAA receptor subunit profiles of tangentially migrating neurons derived from the medial ganglionic eminence. Cereb Cortex, 21(8): 1792–1802

[34] Daw M I, Scott H L, Isaac J T (2007). Developmental synaptic plasticity at the thalamocortical input to barrel cortex: mechanisms and roles. Mol Cell Neurosci, 34(4): 493–502

[35] de Lima A D, Gieseler A, Voigt T (2009). Relationship between GABAergic interneurons migration and early neocortical network activity. Dev Neurobiol, 69(2-3): 105–123

[36] De Marco García N V, Karayannis T, Fishell G (2011). Neuronal activity is required for the development of specific cortical interneuron subtypes. Nature, 472(7343): 351–355

[37] De Marco García N V, Priya R, Tuncdemir S N, Fishell G, Karayannis T (2015). Sensory inputs control the integration of neurogliaform interneurons into cortical circuits. Nat Neurosci, 18(3): 393–401

[38] DeDiego I, Smith-Fernández A, Fairén A (1994). Cortical cells that migrate beyond area boundaries: characterization of an early neuronal population in the lower intermediate zone of prenatal rats. Eur J Neurosci, 6(6): 983–997

[39] Dehorter N, Ciceri G, Bartolini G, Lim L, del Pino I, Marín O (2015). Tuning of fast-spiking interneuron properties by an activity-dependent transcriptional switch. Science, 349(6253): 1216–1220

[40] Denaxa M, Kalaitzidou M, Garefalaki A, Achimastou A, Lasrado R, Maes T, Pachnis V (2012). Maturation-promoting activity of SATB1 in MGE-derived cortical interneurons. Cell Reports, 2(5): 1351–1362

[41] Dupont E, Hanganu I L, Kilb W, Hirsch S, Luhmann H J (2006). Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature, 439(7072): 79–83

[42] Easton C R, Weir K, Scott A, Moen S P, Barger Z, Folch A, Hevner R F, Moody W J (2014). Genetic elimination of GABAergic neurotransmission reveals two distinct pacemakers for spontaneous waves of activity in the developing mouse cortex. J Neurosci, 34(11): 3854–3863

[43] Erzurumlu R S, Gaspar P (2012). Development and critical period plasticity of the barrel cortex. Eur J Neurosci, 35(10): 1540–1553

[44] Espinosa J S, Stryker M P (2012). Development and plasticity of the primary visual cortex. Neuron, 75(2): 230–249

[45] Espinosa J S, Wheeler D G, Tsien R W, Luo L (2009). Uncoupling dendrite growth and patterning: single-cell knockout analysis of NMDA receptor 2B. Neuron, 62(2): 205–217

[46] Feldmeyer D (2012). Excitatory neuronal connectivity in the barrel cortex. Front Neuroanat, 6: 24

[47] Feldmeyer D, Brecht M, Helmchen F, Petersen C C, Poulet J F, Staiger J F, Luhmann H J, Schwarz C (2013). Barrel cortex function. Prog Neurobiol, 103: 3–27

[48] Fishell G, Rudy B (2011). Mechanisms of inhibition within the telencephalon: “where the wild things are”. Annu Rev Neurosci, 34(1): 535–567

[49] Flint A C, Maisch U S, Weishaupt J H, Kriegstein A R, Monyer H (1997). NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci, 17(7): 2469–2476

[50] Frazer S, Otomo K, Dayer A (2015). Early-life serotonin dysregulation affects the migration and positioning of cortical interneuron subtypes. Transl Psychiatry, 5(9): e644

[51] Garaschuk O, Linn J, Eilers J, Konnerth A (2000). Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci, 3(5): 452–459

[52] Gierdalski M, Jablonska B, Siucinska E, Lech M, Skibinska A, Kossut M (2001). Rapid regulation of GAD67 mRNA and protein level in cortical neurons after sensory learning. Cereb Cortex, 11(9): 806–815

[53] Golshani P, Gonçalves J T, Khoshkhoo S, Mostany R, Smirnakis S, Portera-Cailliau C (2009). Internally mediated developmental desynchronization of neocortical network activity. J Neurosci, 29(35): 10890–10899

[54] Hanganu I L, Kilb W, Luhmann H J (2002). Functional synaptic projections onto subplate neurons in neonatal rat somatosensory cortex. J Neurosci, 22(16): 7165–7176

[55] Heck N, Kilb W, Reiprich P, Kubota H, Furukawa T, Fukuda A, Luhmann H J (2007). GABA-A receptors regulate neocortical neuronal migration in vitro and in vivo. Cereb Cortex, 17(1): 138–148

[56] Higashi S, Hioki K, Kurotani T, Kasim N, Molnár Z (2005). Functional thalamocortical synapse reorganization from subplate to layer IV during postnatal development in the reeler-like mutant rat (shaking rat Kawasaki). J Neurosci, 25(6): 1395–1406

[57] Huang Z J, Di Cristo G, Ango F (2007). Development of GABA innervation in the cerebral and cerebellar cortices. Nat Rev Neurosci, 8(9): 673–686

[58] Inada H, Watanabe M, Uchida T, Ishibashi H, Wake H, Nemoto T, Yanagawa Y, Fukuda A, Nabekura J (2011). GABA regulates the multidirectional tangential migration of GABAergic interneurons in living neonatal mice. PLoS ONE, 6(12): e27048

[59] Iwasato T, Datwani A, Wolf A M, Nishiyama H, Taguchi Y, Tonegawa S, Knöpfel T, Erzurumlu R S, Itohara S (2000). Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature, 406(6797): 726–731

[60] Ji X Y, Zingg B, Mesik L, Xiao Z, Zhang L I, Tao H W (2016). Thalamocortical Innervation Pattern in Mouse Auditory and Visual Cortex: Laminar and Cell-Type Specificity. Cereb Cortex, 26(6): 2612–2625

[61] Jiao Y, Zhang C, Yanagawa Y, Sun Q Q (2006). Major effects of sensory experiences on the neocortical inhibitory circuits. J Neurosci, 26(34): 8691–8701

[62] Kanold P O (2004). Transient microcircuits formed by subplate neurons and their role in functional development of thalamocortical connections. Neuroreport, 15(14): 2149–2153

[63] Kanold P O, Kara P, Reid R C, Shatz C J (2003). Role of subplate neurons in functional maturation of visual cortical columns. Science, 301(5632): 521–525

[64] Kanold P O, Luhmann H J (2010). The subplate and early cortical circuits. Annu Rev Neurosci, 33(1): 23–48

[65] Karayannis T, De Marco García N V, Fishell G J (2012). Functional adaptation of cortical interneurons to attenuated activity is subtype-specific. Front Neural Circuits, 6: 66

[66] Karnani M M, Jackson J, Ayzenshtat I, Tucciarone J, Manoocheri K, Snider W G, Yuste R (2016). Cooperative Subnetworks of Molecularly Similar Interneurons in Mouse Neocortex. Neuron, 90(1): 86–100

[67] Kepecs A, Fishell G (2014). Interneuron cell types are fit to function. Nature, 505(7483): 318–326

[68] Khazipov R, Luhmann H J (2006). Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci, 29(7): 414–418

[69] Khazipov R, Sirota A, Leinekugel X, Holmes G L, Ben-Ari Y, Buzsáki G (2004). Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature, 432(7018): 758–761

[70] Kihara M, Yoshioka H, Hirai K, Hasegawa K, Kizaki Z, Sawada T (2002). Stimulation of N-methyl-D-aspartate (NMDA) receptors inhibits neuronal migration in embryonic cerebral cortex: a tissue culture study. Brain Res Dev Brain Res, 138(2): 195–198

[71] Kilb W, Kirischuk S, Luhmann H J (2011). Electrical activity patterns and the functional maturation of the neocortex. Eur J Neurosci, 34(10): 1677–1686

[72] Kilb W, Kirischuk S, Luhmann H J (2013). Role of tonic GABAergic currents during pre- and early postnatal rodent development. Front Neural Circuits, 7: 139

[73] Killackey H P (1973). Anatomical evidence for cortical subdivisions based on vertically discrete thalamic projections from the ventral posterior nucleus to cortical barrels in the rat. Brain Res, 51: 326–331

[74] Kirmse K, Kummer M, Kovalchuk Y, Witte O W, Garaschuk O, Holthoff K (2015). GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo. Nat Commun, 6: 7750

[75] Koolen N, Dereymaeker A, Räsänen O, Jansen K, Vervisch J, Matic V, Naulaers G, De Vos M, Van Huffel S, Vanhatalo S (2016). Early development of synchrony in cortical activations in the human. Neuroscience, 322: 298–307

[76] Kral A (2013). Auditory critical periods: a review from system’s perspective. Neuroscience, 247: 117–133

[77] Laaris N, Carlson G C, Keller A (2000). Thalamic-evoked synaptic interactions in barrel cortex revealed by optical imaging. J Neurosci, 20(4): 1529–1537

[78] Lee L J, Iwasato T, Itohara S, Erzurumlu R S (2005). Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice. J Comp Neurol, 485(4): 280–292

[79] Lewis D A (2014). Inhibitory neurons in human cortical circuits: substrate for cognitive dysfunction in schizophrenia. Curr Opin Neurobiol, 26: 22–26

[80] Li H, Fertuzinhos S, Mohns E, Hnasko T S, Verhage M, Edwards R, Sestan N, Crair M C (2013). Laminar and columnar development of barrel cortex relies on thalamocortical neurotransmission. Neuron, 79(5): 970–986

[81] Liang F, Isackson P J, Jones E G (1996). Stimulus-dependent, reciprocal up- and downregulation of glutamic acid decarboxylase and Ca²⁺/calmodulin-dependent protein kinase II gene expression in rat cerebral cortex. Exp Brain Res, 110(2): 163–174

[82] Liodis P, Denaxa M, Grigoriou M, Akufo-Addo C, Yanagawa Y, Pachnis V (2007). Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J Neurosci, 27(12): 3078–3089

[83] Liu X, Hashimoto-Torii K, Torii M, Ding C, Rakic P (2010). Gap junctions/hemichannels modulate interkinetic nuclear migration in the forebrain precursors. J Neurosci, 30(12): 4197–4209

[84] Liu X, Hashimoto-Torii K, Torii M, Haydar T F, Rakic P (2008). The role of ATP signaling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone. Proc Natl Acad Sci USA, 105(33): 11802–11807

[85] Liu X B, Murray K D, Jones E G (2004). Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J Neurosci, 24(40): 8885–8895

[86] Lorente de No R (1922). La Corteza Cerebral del Raton (Primera Contribucion- La Corteza Acustica). Trabajos del Laboratorio de Investigaciones Biologicas, 20: 41–78

[87] LoTurco J J, Blanton M G, Kriegstein A R (1991). Initial expression and endogenous activation of NMDA channels in early neocortical development. J Neurosci, 11(3): 792–799

[88] Luhmann H J, Fukuda A, Kilb W (2015). Control of cortical neuronal migration by glutamate and GABA. Front Cell Neurosci, 9: 4

[89] Luhmann H J, Hanganu I, Kilb W (2003). Cellular physiology of the neonatal rat cerebral cortex. Brain Res Bull, 60(4): 345–353

[90] Luhmann H J, Kirischuk S, Sinning A, Kilb W (2014). Early GABAergic circuitry in the cerebral cortex. Curr Opin Neurobiol, 26: 72–78

[91] Manent J B, Jorquera I, Ben-Ari Y, Aniksztejn L, Represa A (2006). Glutamate acting on AMPA but not NMDA receptors modulates the migration of hippocampal interneurons. J Neurosci, 26(22): 5901–5909

[92] Marín O (2012). Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci, 13(2): 107–120

[93] Marques-Smith A, Lyngholm D, Kaufmann A K, Stacey J A, Hoerder-Suabedissen A, Becker E B, Wilson M C, Molnár Z, Butt S J (2016). A Transient Translaminar GABAergic Interneuron Circuit Connects Thalamocortical Recipient Layers in Neonatal Somatosensory Cortex. Neuron, 89(3): 536–549

[94] Matta J A, Pelkey K A, Craig M T, Chittajallu R, Jeffries B W, McBain C J (2013). Developmental origin dictates interneuron AMPA and NMDA receptor subunit composition and plasticity. Nat Neurosci, 16(8): 1032–1041

[95] McCabe A K, Chisholm S L, Picken-Bahrey H L, Moody W J (2006). The self-regulating nature of spontaneous synchronized activity in developing mouse cortical neurones. J Physiol, 577(Pt 1): 155–167

[96] 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(7): 1582–1594

[97] Minlebaev M, Ben-Ari Y, Khazipov R (2007). Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J Neurophysiol, 97(1): 692–700

[98] Minlebaev M, Ben-Ari Y, Khazipov R (2009). NMDA receptors pattern early activity in the developing barrel cortex in vivo. Cereb Cortex, 19(3): 688–696

[99] Minlebaev M, Colonnese M, Tsintsadze T, Sirota A, Khazipov R (2011). Early g oscillations synchronize developing thalamus and cortex. Science, 334(6053): 226–229

[100] Mix A, Hoppenrath K, Funke K (2015). Reduction in cortical parvalbumin expression due to intermittent theta-burst stimulation correlates with maturation of the perineuronal nets in young rats. Dev Neurobiol, 75(1): 1–11

[101] Miyashita-Lin E M, Hevner R, Wassarman K M, Martinez S, Rubenstein J L (1999). Early neocortical regionalization in the absence of thalamic innervation. Science, 285(5429): 906–909

[102] Miyoshi G, Butt S J, Takebayashi H, Fishell G (2007). Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J Neurosci, 27(29): 7786–7798

[103] Miyoshi G, Fishell G (2011). GABAergic interneuron lineages selectively sort into specific cortical layers during early postnatal development. Cereb Cortex, 21(4): 845–852

[104] Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa V H, Butt S J, Battiste J, Johnson J E, Machold R P, Fishell G (2010). Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci, 30(5): 1582–1594

[105] Mizuno H, Luo W, Tarusawa E, Saito Y M, Sato T, Yoshimura Y, Itohara S, Iwasato T (2014). NMDAR-regulated dynamics of layer 4 neuronal dendrites during thalamocortical reorganization in neonates. Neuron, 82(2): 365–379

[106] Molnár Z, Adams R, Blakemore C (1998). Mechanisms underlying the early establishment of thalamocortical connections in the rat. J Neurosci, 18(15): 5723–5745

[107] Murthy S, Niquille M, Hurni N, Limoni G, Frazer S, Chameau P, van Hooft J A, Vitalis T, Dayer A (2014). Serotonin receptor 3A controls interneuron migration into the neocortex. Nat Commun, 5: 5524

[108] Narboux-Nême N, Evrard A, Ferezou I, Erzurumlu R S, Kaeser P S, Lainé J, Rossier J, Ropert N, Südhof T C, Gaspar P (2012). Neurotransmitter release at the thalamocortical synapse instructs barrel formation but not axon patterning in the somatosensory cortex. J Neurosci, 32(18): 6183–6196

[109] Oh W C, Lutzu S, Castillo P E, Kwon H B (2016). De novo synaptogenesis induced by GABA in the developing mouse cortex. Science, 353(6303): 1037–1040

[110] Okaty B W, Miller M N, Sugino K, Hempel C M, Nelson S B (2009). Transcriptional and electrophysiological maturation of neocortical fast-spiking GABAergic interneurons. J Neurosci, 29(21): 7040–7052

[111] Paoletti P, Bellone C, Zhou Q (2013). NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci, 14(6): 383–400

[112] Petersen C C (2007). The functional organization of the barrel cortex. Neuron, 56(2): 339–355

[113] Porter J T, Johnson C K, Agmon A (2001). Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J Neurosci, 21(8): 2699–2710

[114] Reiprich P, Kilb W, Luhmann H J (2005). Neonatal NMDA receptor blockade disturbs neuronal migration in rat somatosensory cortex in vivo. Cereb Cortex, 15(3): 349–358

[115] Rheims S, Minlebaev M, Ivanov A, Represa A, Khazipov R, Holmes G L, Ben-Ari Y, Zilberter Y (2008). Excitatory GABA in rodent developing neocortex in vitro. J Neurophysiol, 100(2): 609–619

[116] Riccio O, Potter G, Walzer C, Vallet P, Szabó G, Vutskits L, Kiss J Z, Dayer A G (2009). Excess of serotonin affects embryonic interneuron migration through activation of the serotonin receptor 6. Mol Psychiatry, 14(3): 280–290

[117] 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(1): 45–61

[118] Rutherford L C, DeWan A, Lauer H M, Turrigiano G G (1997). Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures. J Neurosci, 17(12): 4527–4535

[119] Sanes D H, Kotak V C (2011). Developmental plasticity of auditory cortical inhibitory synapses. Hear Res, 279(1-2): 140–148

[120] Schwartz T H, Rabinowitz D, Unni V, Kumar V S, Smetters D K, Tsiola A, Yuste R (1998). Networks of coactive neurons in developing layer 1. Neuron, 20(3): 541–552

[121] Siegel F, Heimel J A, Peters J, Lohmann C (2012). Peripheral and central inputs shape network dynamics in the developing visual cortex in vivo. Curr Biol, 22(3): 253–258

[122] Sippy T, Yuste R (2013). Decorrelating action of inhibition in neocortical networks. J Neurosci, 33(23): 9813–9830

[123] Soria J M, Valdeolmillos M (2002). Receptor-activated calcium signals in tangentially migrating cortical cells. Cereb Cortex, 12(8): 831–839

[124] Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003). In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci USA, 100(12): 7319–7324

[125] Sultan K T, Brown K N, Shi S H (2013). Production and organization of neocortical interneurons. Front Cell Neurosci, 7: 221

[126] Sun J J, Luhmann H J (2007). Spatio-temporal dynamics of oscillatory network activity in the neonatal mouse cerebral cortex. Eur J Neurosci, 26(7): 1995–2004

[127] Sun Q Q, Huguenard J R, Prince D A (2006). Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J Neurosci, 26(4): 1219–1230

[128] Sur M, Leamey C A (2001). Development and plasticity of cortical areas and networks. Nat Rev Neurosci, 2(4): 251–262

[129] Takano T (2015). Interneuron Dysfunction in Syndromic Autism: Recent Advances. Dev Neurosci, 37(6): 467–475

[130] Tasic B, Menon V, Nguyen T N, Kim T K, Jarsky T, Yao Z, Levi B, Gray L T, Sorensen S A, Dolbeare T, Bertagnolli D, Goldy J, Shapovalova N, Parry S, Lee C, Smith K, Bernard A, Madisen L, Sunkin S M, Hawrylycz M, Koch C, Zeng H (2016). Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat Neurosci, 19(2): 335–346

[131] Tolner E A, Sheikh A, Yukin A Y, Kaila K, Kanold P O (2012). Subplate neurons promote spindle bursts and thalamocortical patterning in the neonatal rat somatosensory cortex. J Neurosci, 32(2): 692–702

[132] Tolonen M, Palva J M, Andersson S, Vanhatalo S (2007). Development of the spontaneous activity transients and ongoing cortical activity in human preterm babies. Neuroscience, 145(3): 997–1006

[133] Trevelyan A J, Muldoon S F, Merricks E M, Racca C, Staley K J (2015). The role of inhibition in epileptic networks. J Clin Neurophysiol, 32(3): 227–234

[134] Tuncdemir S N, Wamsley B, Stam F J, Osakada F, Goulding M, Callaway E M, Rudy B, Fishell G (2016). Early Somatostatin Interneuron Connectivity Mediates the Maturation of Deep Layer Cortical Circuits. Neuron, 89(3): 521–535

[135] Uhlén P, Fritz N, Smedler E, Malmersjö S, Kanatani S (2015). Calcium signaling in neocortical development. Dev Neurobiol, 75(4): 360–368

[136] Van der Loos H, Woolsey T A (1973). Somatosensory cortex: structural alterations following early injury to sense organs. Science, 179(4071): 395–398

[137] Van Eden C G, Mrzljak L, Voorn P, Uylings H B (1989). Prenatal development of GABA-ergic neurons in the neocortex of the rat. J Comp Neurol, 289(2): 213–227

[138] Vitalis T, Ansorge M S, Dayer A G (2013). Serotonin homeostasis and serotonin receptors as actors of cortical construction: special attention to the 5-HT3A and 5-HT6 receptor subtypes. Front Cell Neurosci, 7: 93

[139] Vitalis T, Cases O, Passemard S, Callebert J, Parnavelas J G (2007). Embryonic depletion of serotonin affects cortical development. Eur J Neurosci, 26(2): 331–344

[140] Voigt T, Opitz T, de Lima A D (2001). Synchronous oscillatory activity in immature cortical network is driven by GABAergic preplate neurons. J Neurosci, 21(22): 8895–8905

[141] Welker C (1971). Microelectrode delineation of fine grain somatotopic organization of (SmI) cerebral neocortex in albino rat. Brain Res, 26(2): 259–275

[142] Welker C (1976). Receptive fields of barrels in the somatosensory neocortex of the rat. J Comp Neurol, 166(2): 173–189

[143] White L E, Fitzpatrick D (2007). Vision and cortical map development. Neuron, 56(2): 327–338

[144] Wichterle H, Garcia-Verdugo J M, Herrera D G, Alvarez-Buylla A (1999). Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci, 2(5): 461–466

[145] Wichterle H, Turnbull D H, Nery S, Fishell G, Alvarez-Buylla A (2001). In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development, 128(19): 3759–3771

[146] Woolsey T A, Van der Loos H (1970). The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res, 17(2): 205–242

[147] Wu X, Fu Y, Knott G, Lu J, Di Cristo G, Huang Z J (2012). GABA signaling promotes synapse elimination and axon pruning in developing cortical inhibitory interneurons. J Neurosci, 32(1): 331–343

[148] Yang J W, Hanganu-Opatz I L, Sun J J, Luhmann H J (2009). Three patterns of oscillatory activity differentially synchronize developing neocortical networks in vivo. J Neurosci, 29(28): 9011–9025

[149] Yang J W, Reyes-Puerta V, Kilb W, Luhmann H J (2016). Spindle Bursts in Neonatal Rat Cerebral Cortex. Neural Plast, 2016: 3467832

[150] Yozu M, Tabata H, Konig N, Nakajima K (2008). Migratory behavior of presumptive interneurons is affected by AMPA receptor activation in slice cultures of embryonic mouse neocortex. Dev Neurosci, 30(1-3): 105–116

[151] Zeisel A, Muñoz-Manchado A B, Codeluppi S, Lönnerberg P, La Manno G, Juréus A, Marques S, Munguba H, He L, Betsholtz C, Rolny C, Castelo-Branco G, Hjerling-Leffler J, Linnarsson S (2015). Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science, 347(6226): 1138–1142

[152] Zhang Z, Sun Q Q (2011). Development of NMDA NR2 subunits and their roles in critical period maturation of neocortical GABAergic interneurons. Dev Neurobiol, 71(3): 221–245

Acknowledgements

We are grateful to A. Che, P. Chu, and S. Z. Duan for comments on the manuscript. N.V.D.M.G. is supported by grants from the National Institutes of Health (5 R00 MH095825 05; 1 R01 MH110553 01), the Leon Levy Foundation, and Citizens United for Research in Epilepsy (CURE). R.B. is supported by a Medical Scientist Training Program grant from the National Institute of General Medical Sciences of the NIH under award number T32GM07739 to the Weill Cornell/Rockefeller/Sloan-Kettering Tri-Institutional MD-PhD Program.

Compliance with ethics guidelines

Rachel Babij, Natalia De Marco Garcia declare that they have no conflict of interest. This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

2016 Higher Education Press and Springer-Verlag Berlin Heidelberg