A Transient Translaminar GABAergic Interneuron Circuit Connects Thalamocortical Recipient Layers in Neonatal Somatosensory Cortex

Neuron

Volumn 89, Issue 3, 2016, Pages 536-549

  Marques Smith, Andre ^a,c   Lyngholm, Daniel ^a,d   Kaufmann, Anna Kristin ^a,e   Stacey, Jacqueline A ^a   Hoerder Suabedissen, Anna ^a   Becker, Esther B E ^a   Wilson, Michael C ^b   Molnár, Zoltán ^a   Butt, Simon J B ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^e MRC Anat Neuropharmacology Unit   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; NEU DIFFERENTIATION FACTOR; PURINERGIC P2X2 RECEPTOR; 4 AMINOBUTYRIC ACID; NRG1 PROTEIN, MOUSE; SOMATOSTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CAPSULA INTERNA; DEVELOPMENTAL STAGE; INFRAORBITAL NERVE; INNERVATION; LONG TERM POTENTIATION; MOUSE; NEOCORTEX; NERVE CELL EXCITABILITY; NEUROTRANSMISSION; NONHUMAN; PERINATAL PERIOD; PHOTOSTIMULATION; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; SOMATOSENSORY CORTEX; STIMULUS RESPONSE; SYNAPSE; TELENCEPHALON; THALAMOCORTICAL TRACT; THALAMUS; UPREGULATION; ANIMAL; BIOSYNTHESIS; CYTOLOGY; ELECTROSTIMULATION; FEMALE; GROWTH, DEVELOPMENT AND AGING; INTERNEURON; MALE; MEMBRANE POTENTIAL; NERVE TRACT; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ELECTRIC STIMULATION; FEMALE; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; MALE; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; NEURAL PATHWAYS; NEUREGULIN-1; PHOTIC STIMULATION; SOMATOSENSORY CORTEX; SOMATOSTATIN; THALAMUS;

EID: 84959314305     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.01.015     Document Type: Article

References (91)

1. Agmon A., Connors B.W. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 1991, 41:365-379.
2. Agmon A., Hollrigel G., O'Dowd D.K. Functional GABAergic synaptic connection in neonatal mouse barrel cortex. J. Neurosci. 1996, 16:4684-4695.
3. Allendoerfer K.L., Shatz C.J. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu. Rev. Neurosci. 1994, 17:185-218.
4. An S., Yang J.W., Sun H., Kilb W., Luhmann H.J. Long-term potentiation in the neonatal rat barrel cortex in vivo. J. Neurosci. 2012, 32:9511-9516.
5. An S., Kilb W., Luhmann H.J. Sensory-evoked and spontaneous gamma and spindle bursts in neonatal rat motor cortex. J. Neurosci. 2014, 34:10870-10883.
6. Anastasiades P.G., Butt S.J. A role for silent synapses in the development of the pathway from layer 2/3 to 5 pyramidal cells in the neocortex. J. Neurosci. 2012, 32:13085-13099.
7. Anastasiades P.G., Marques-Smith S., Lyngholm D., Lickiss T., Raffiq S., Kätzel D., Miesenböck G., Butt S.J.B. GABAergic interneurons form transient, layer-specific circuits in early postnatal neocortex. Nat. Commun. 2016, 7. 10.1038/ncomms10584.
8. Ben-Ari Y., Khalilov I., Represa A., Gozlan H. Interneurons set the tune of developing networks. Trends Neurosci. 2004, 27:422-427.
9. Bloodgood B.L., Sharma N., Browne H.A., Trepman A.Z., Greenberg M.E. The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition. Nature 2013, 503:121-125.
10. Bortone D.S., Olsen S.R., Scanziani M. Translaminar inhibitory cells recruited by layer 6 corticothalamic neurons suppress visual cortex. Neuron 2014, 82:474-485.
11. Buchanan K.A., Blackman A.V., Moreau A.W., Elgar D., Costa R.P., Lalanne T., Tudor Jones A.A., Oyrer J., Sjöström P.J. Target-specific expression of presynaptic NMDA receptors in neocortical microcircuits. Neuron 2012, 75:451-466.
12. Butt S.J., Fuccillo M., Nery S., Noctor S., Kriegstein A., Corbin J.G., Fishell G. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 2005, 48:591-604.
13. Callaway E.M., Borrell V. Developmental sculpting of dendritic morphology of layer 4 neurons in visual cortex: influence of retinal input. J. Neurosci. 2011, 31:7456-7470.
14. Chattopadhyaya B., Di Cristo G., Higashiyama H., Knott G.W., Kuhlman S.J., Welker E., Huang Z.J. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J. Neurosci. 2004, 24:9598-9611.
15. Chittajallu R., Isaac J.T. Emergence of cortical inhibition by coordinated sensory-driven plasticity at distinct synaptic loci. Nat. Neurosci. 2010, 13:1240-1248.
16. Chou S.J., Babot Z., Leingärtner A., Studer M., Nakagawa Y., O'Leary D.D. Geniculocortical input drives genetic distinctions between primary and higher-order visual areas. Science 2013, 340:1239-1242.
17. Close J., Xu H., De Marco García N., Batista-Brito R., Rossignol E., Rudy B., Fishell G. Satb1 is an activity-modulated transcription factor required for the terminal differentiation and connectivity of medial ganglionic eminence-derived cortical interneurons. J. Neurosci. 2012, 32:17690-17705.
18. Crair M.C., Malenka R.C. A critical period for long-term potentiation at thalamocortical synapses. Nature 1995, 375:325-328.
19. Crocker-Buque A., Brown S.M., Kind P.C., Isaac J.T., Daw M.I. Experience-dependent, layer-specific development of divergent thalamocortical connectivity. Cereb. Cortex 2015, 25:2255-2266.
20. Cruikshank S.J., Urabe H., Nurmikko A.V., Connors B.W. Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 2010, 65:230-245.
21. Daw M.I., Ashby M.C., Isaac J.T. Coordinated developmental recruitment of latent fast spiking interneurons in layer IV barrel cortex. Nat. Neurosci. 2007, 10:453-461.
22. De la Rossa A., Bellone C., Golding B., Vitali I., Moss J., Toni N., Lüscher C., Jabaudon D. In vivo reprogramming of circuit connectivity in postmitotic neocortical neurons. Nat. Neurosci. 2013, 16:193-200.
23. Deakin I.H., Law A.J., Oliver P.L., Schwab M.H., Nave K.A., Harrison P.J., Bannerman D.M. Behavioural characterization of neuregulin 1 type I overexpressing transgenic mice. Neuroreport 2009, 20:1523-1528.
24. Deakin I.H., Nissen W., Law A.J., Lane T., Kanso R., Schwab M.H., Nave K.A., Lamsa K.P., Paulsen O., Bannerman D.M., Harrison P.J. Transgenic overexpression of the type I isoform of neuregulin 1 affects working memory and hippocampal oscillations but not long-term potentiation. Cereb. Cortex 2012, 22:1520-1529.
25. Donato F., Rompani S.B., Caroni P. Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 2013, 504:272-276.
26. Dupont E., Hanganu I.L., Kilb W., Hirsch S., Luhmann H.J. Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature 2006, 439:79-83.
27. Elgazzar R.F., Mutabagani M.A., Abdelaal S.E., Sadakah A.A. Platelet rich plasma may enhance peripheral nerve regeneration after cyanoacrylate reanastomosis: a controlled blind study on rats. Int. J. Oral Maxillofac. Surg. 2008, 37:748-755.
28. Erzurumlu R.S., Gaspar P. Development and critical period plasticity of the barrel cortex. Eur. J. Neurosci. 2012, 35:1540-1553.
29. Fazzari P., Paternain A.V., Valiente M., Pla R., Luján R., Lloyd K., Lerma J., Marín O., Rico B. Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 2010, 464:1376-1380.
30. Friauf E., McConnell S.K., Shatz C.J. Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex. J. Neurosci. 1990, 10:2601-2613.
31. Gil Z., Amitai Y. Properties of convergent thalamocortical and intracortical synaptic potentials in single neurons of neocortex. J. Neurosci. 1996, 16:6567-6578.
32. Gil Z., Connors B.W., Amitai Y. Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 1999, 23:385-397.
33. Hanganu I.L., Kilb W., Luhmann H.J. Functional synaptic projections onto subplate neurons in neonatal rat somatosensory cortex. J. Neurosci. 2002, 22:7165-7176.
34. Higashi S., Crair M.C., Kurotani T., Inokawa H., Toyama K. Altered spatial patterns of functional thalamocortical connections in the barrel cortex after neonatal infraorbital nerve cut revealed by optical recording. Neuroscience 1999, 91:439-452.
35. Higashi S., Molnár Z., Kurotani T., Toyama K. Prenatal development of neural excitation in rat thalamocortical projections studied by optical recording. Neuroscience 2002, 115:1231-1246.
36. Hoerder-Suabedissen A., Molnár Z. Molecular diversity of early-born subplate neurons. Cereb. Cortex 2013, 23:1473-1483.
37. Hubel D.H., Wiesel T.N. Effects of monocular deprivation in kittens. Naunyn Schmiedebergs Arch. Exp. Pathol. Pharmakol. 1964, 248:492-497.
38. Hubel D.H., Wiesel T.N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 1970, 206:419-436.
39. Isaac J.T., Crair M.C., Nicoll R.A., Malenka R.C. Silent synapses during development of thalamocortical inputs. Neuron 1997, 18:269-280.
40. Jiao Y., Zhang C., Yanagawa Y., Sun Q.Q. Major effects of sensory experiences on the neocortical inhibitory circuits. J. Neurosci. 2006, 26:8691-8701.
41. Kanold P.O., Luhmann H.J. The subplate and early cortical circuits. Annu. Rev. Neurosci. 2010, 33:23-48.
42. Kanold P.O., Shatz C.J. Subplate neurons regulate maturation of cortical inhibition and outcome of ocular dominance plasticity. Neuron 2006, 51:627-638.
43. Kanold P.O., Kara P., Reid R.C., Shatz C.J. Role of subplate neurons in functional maturation of visual cortical columns. Science 2003, 301:521-525.
44. Kasper E.M., Lübke J., Larkman A.U., Blakemore C. Pyramidal neurons in layer 5 of the rat visual cortex. III. Differential maturation of axon targeting, dendritic morphology, and electrophysiological properties. J. Comp. Neurol. 1994, 339:495-518.
45. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
46. Kätzel D., Miesenböck G. Experience-dependent rewiring of specific inhibitory connections in adult neocortex. PLoS Biol. 2014, 12:e1001798.
47. Kätzel D., Zemelman B.V., Buetfering C., Wölfel M., Miesenböck G. The columnar and laminar organization of inhibitory connections to neocortical excitatory cells. Nat. Neurosci. 2011, 14:100-107.
48. Khazipov R., Sirota A., Leinekugel X., Holmes G.L., Ben-Ari Y., Buzsáki G. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 2004, 432:758-761.
49. Koester S.E., O'Leary D.D. Functional classes of cortical projection neurons develop dendritic distinctions by class-specific sculpting of an early common pattern. J. Neurosci. 1992, 12:1382-1393.
50. König N., Roch G., Marty R. The onset of synaptogenesis in rat temporal cortex. Anat. Embryol. (Berl.) 1975, 148:73-87.
51. Li H., Fertuzinhos S., Mohns E., Hnasko T.S., Verhage M., Edwards R., Sestan N., Crair M.C. Laminar and columnar development of barrel cortex relies on thalamocortical neurotransmission. Neuron 2013, 79:970-986.
52. Luhmann H.J., Kilb W., Hanganu-Opatz I.L. Subplate cells: amplifiers of neuronal activity in the developing cerebral cortex. Front. Neuroanat. 2009, 3:19.
53. Luhmann H.J., Kirischuk S., Sinning A., Kilb W. Early GABAergic circuitry in the cerebral cortex. Curr. Opin. Neurobiol. 2014, 26:72-78.
54. Matsui A., Tran M., Yoshida A.C., Kikuchi S.S., U M., Ogawa M., Shimogori T. BTBD3 controls dendrite orientation toward active axons in mammalian neocortex. Science 2013, 342:1114-1118.
55. Michailov G.V., Sereda M.W., Brinkmann B.G., Fischer T.M., Haug B., Birchmeier C., Role L., Lai C., Schwab M.H., Nave K.A. Axonal neuregulin-1 regulates myelin sheath thickness. Science 2004, 304:700-703.
56. Miesenböck G. Optogenetic control of cells and circuits. Annu. Rev. Cell Dev. Biol. 2011, 27:731-758.
57. Minlebaev M., Ben-Ari Y., Khazipov R. Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J. Neurophysiol. 2007, 97:692-700.
58. Minlebaev M., Ben-Ari Y., Khazipov R. NMDA receptors pattern early activity in the developing barrel cortex in vivo. Cereb. Cortex 2009, 19:688-696.
59. Minlebaev M., Colonnese M., Tsintsadze T., Sirota A., Khazipov R. Early γ oscillations synchronize developing thalamus and cortex. Science 2011, 334:226-229.
60. Miyoshi G., Butt S.J., Takebayashi H., Fishell G. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J. Neurosci. 2007, 27:7786-7798.
61. Owens D.F., Liu X., Kriegstein A.R. Changing properties of GABA(A) receptor-mediated signaling during early neocortical development. J. Neurophysiol. 1999, 82:570-583.
62. Pangratz-Fuehrer S., Hestrin S. Synaptogenesis of electrical and GABAergic synapses of fast-spiking inhibitory neurons in the neocortex. J. Neurosci. 2011, 31:10767-10775.
63. Piñon M.C., Jethwa A., Jacobs E., Campagnoni A., Molnár Z. Dynamic integration of subplate neurons into the cortical barrel field circuitry during postnatal development in the Golli-tau-eGFP (GTE) mouse. J. Physiol. 2009, 587:1903-1915.
64. Porter J.T., Johnson C.K., Agmon A. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J. Neurosci. 2001, 21:2699-2710.
65. Pouchelon G., Gambino F., Bellone C., Telley L., Vitali I., Lüscher C., Holtmaat A., Jabaudon D. Modality-specific thalamocortical inputs instruct the identity of postsynaptic L4 neurons. Nature 2014, 511:471-474.
66. Raastad M., Storm J.F., Andersen P. Putative single quantum and single fibre excitatory postsynaptic currents show similar amplitude range and variability in rat hippocampal slices. Eur. J. Neurosci. 1992, 4:113-117.
67. Sadaka Y., Weinfeld E., Lev D.L., White E.L. Changes in mouse barrel synapses consequent to sensory deprivation from birth. J. Comp. Neurol. 2003, 457:75-86.
68. Salami M., Itami C., Tsumoto T., Kimura F. Change of conduction velocity by regional myelination yields constant latency irrespective of distance between thalamus and cortex. Proc. Natl. Acad. Sci. USA 2003, 100:6174-6179.
69. Spiegel I., Mardinly A.R., Gabel H.W., Bazinet J.E., Couch C.H., Tzeng C.P., Harmin D.A., Greenberg M.E. Npas4 regulates excitatory-inhibitory balance within neural circuits through cell-type-specific gene programs. Cell 2014, 157:1216-1229.
70. Sugiyama S., Di Nardo A.A., Aizawa S., Matsuo I., Volovitch M., Prochiantz A., Hensch T.K. Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 2008, 134:508-520.
71. Takesian A.E., Kotak V.C., Sanes D.H. Presynaptic GABA(B) receptors regulate experience-dependent development of inhibitory short-term plasticity. J. Neurosci. 2010, 30:2716-2727.
72. Takesian A.E., Kotak V.C., Sharma N., Sanes D.H. Hearing loss differentially affects thalamic drive to two cortical interneuron subtypes. J. Neurophysiol. 2013, 110:999-1008.
73. Tan Z., Hu H., Huang Z.J., Agmon A. Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons. Proc. Natl. Acad. Sci. USA 2008, 105:2187-2192.
74. Tang Y., Stryker M.P., Alvarez-Buylla A., Espinosa J.S. Cortical plasticity induced by transplantation of embryonic somatostatin or parvalbumin interneurons. Proc. Natl. Acad. Sci. USA 2014, 111:18339-18344.
75. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Fu Y., Lu J., Lin Y., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
76. Tolner E.A., Sheikh A., Yukin A.Y., Kaila K., Kanold P.O. Subplate neurons promote spindle bursts and thalamocortical patterning in the neonatal rat somatosensory cortex. J. Neurosci. 2012, 32:692-702.
77. Tuncdemir S.N., Wamsley B., Stam F.J., Osakada F., Goulding M., Callaway E.M., Rudy B., Fishell G. Early somatostatin interneuron connectivity mediates the maturation of deep layer cortical circuits. Neuron 2016, 89:521-535. this issue.
78. Van der Loos H., Woolsey T.A. Somatosensory cortex: structural alterations following early injury to sense organs. Science 1973, 179:395-398.
79. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., Toonen R.F., Hammer R.E., van den Berg T.K., Missler M., et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 2000, 287:864-869.
80. Vue T.Y., Lee M., Tan Y.E., Werkhoven Z., Wang L., Nakagawa Y. Thalamic control of neocortical area formation in mice. J. Neurosci. 2013, 33:8442-8453.
81. Wang Y., Toledo-Rodriguez M., Gupta A., Wu C., Silberberg G., Luo J., Markram H. Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J. Physiol. 2004, 561:65-90.
82. Washbourne P., Thompson P.M., Carta M., Costa E.T., Mathews J.R., Lopez-Benditó G., Molnár Z., Becher M.W., Valenzuela C.F., Partridge L.D., Wilson M.C. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 2002, 5:19-26.
83. West D.C., Mercer A., Kirchhecker S., Morris O.T., Thomson A.M. Layer 6 cortico-thalamic pyramidal cells preferentially innervate interneurons and generate facilitating EPSPs. Cereb. Cortex 2006, 16:200-211.
84. Xu X., Callaway E.M. Laminar specificity of functional input to distinct types of inhibitory cortical neurons. J. Neurosci. 2009, 29:70-85.
85. Xu H., Jeong H.Y., Tremblay R., Rudy B. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 2013, 77:155-167.
86. Xue M., Atallah B.V., Scanziani M. Equalizing excitation-inhibition ratios across visual cortical neurons. Nature 2014, 511:596-600.
87. Yang J.W., Hanganu-Opatz I.L., Sun J.J., Luhmann H.J. Three patterns of oscillatory activity differentially synchronize developing neocortical networks in vivo. J. Neurosci. 2009, 29:9011-9025.
88. Yang J.W., An S., Sun J.J., Reyes-Puerta V., Kindler J., Berger T., Kilb W., Luhmann H.J. Thalamic network oscillations synchronize ontogenetic columns in the newborn rat barrel cortex. Cereb. Cortex 2013, 23:1299-1316.
89. Yang W., Carrasquillo Y., Hooks B.M., Nerbonne J.M., Burkhalter A. Distinct balance of excitation and inhibition in an interareal feedforward and feedback circuit of mouse visual cortex. J. Neurosci. 2013, 33:17373-17384.
90. Zemelman B.V., Nesnas N., Lee G.A., Miesenbock G. Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. Proc. Natl. Acad. Sci. USA 2003, 100:1352-1357.
91. Zhao C., Kao J.P., Kanold P.O. Functional excitatory microcircuits in neonatal cortex connect thalamus and layer 4. J. Neurosci. 2009, 29:15479-15488.