1932

Abstract

Cortical interneurons display striking differences in shape, physiology, and other attributes, challenging us to appropriately classify them. We previously suggested that interneuron types should be defined by their role in cortical processing. Here, we revisit the question of how to codify their diversity based upon their division of labor and function as controllers of cortical information flow. We suggest that developmental trajectories provide a guide for appreciating interneuron diversity and argue that subtype identity is generated using a configurational (rather than combinatorial) code of transcription factors that produce attractor states in the underlying gene regulatory network. We present our updated three-stage model for interneuron specification: an initial cardinal step, allocating interneurons into a few major classes, followed by definitive refinement, creating subclasses upon settling within the cortex, and lastly, state determination, reflecting the incorporation of interneurons into functional circuit ensembles. We close by discussing findings indicating that major interneuron classes are both evolutionarily ancient and conserved. We propose that the complexity of cortical circuits is generated by phylogenetically old interneuron types, complemented by an evolutionary increase in principal neuron diversity. This suggests that a natural neurobiological definition of interneuron types might be derived from a match between their developmental origin and computational function.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-070918-050421
2020-07-08
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/neuro/43/1/annurev-neuro-070918-050421.html?itemId=/content/journals/10.1146/annurev-neuro-070918-050421&mimeType=html&fmt=ahah

Literature Cited

  1. Adesnik H, Bruns W, Taniguchi H, Huang ZJ, Scanziani M 2012. A neural circuit for spatial summation in visual cortex. Nature 490:226–31
    [Google Scholar]
  2. Alitto HJ, Dan Y. 2012. Cell-type-specific modulation of neocortical activity by basal forebrain input. Front. Syst. Neurosci. 6:79
    [Google Scholar]
  3. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL 1997. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474–76
    [Google Scholar]
  4. Andersson E, Tryggvason U, Deng Q, Friling S, Alekseenko Z et al. 2006. Identification of intrinsic determinants of midbrain dopamine neurons. Cell 124:393–405
    [Google Scholar]
  5. Atallah BV, Bruns W, Carandini M, Scanziani M 2012. Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73:159–70
    [Google Scholar]
  6. Attinger A, Wang B, Keller GB 2017. Visuomotor coupling shapes the functional development of mouse visual cortex. Cell 169:1291–302.e14
    [Google Scholar]
  7. Au E, Ahmed T, Karayannis T, Biswas S, Gan L, Fishell G 2013. A modular gain-of-function approach to generate cortical interneuron subtypes from ES cells. Neuron 80:1145–58
    [Google Scholar]
  8. Azim E, Jabaudon D, Fame RM, Macklis JD 2009. SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development. Nat. Neurosci. 12:1238–47
    [Google Scholar]
  9. Bandler RC, Mayer C, Fishell G 2017. Cortical interneuron specification: the juncture of genes, time and geometry. Curr. Opin. Neurobiol. 42:17–24
    [Google Scholar]
  10. Batista-Brito R, Fishell G. 2009. The developmental integration of cortical interneurons into a functional network. Curr. Top. Dev. Biol. 87:81–118
    [Google Scholar]
  11. Batista-Brito R, Rossignol E, Hjerling-Leffler J, Denaxa M, Wegner M et al. 2009. The cell-intrinsic requirement of Sox6 for cortical interneuron development. Neuron 63:466–81
    [Google Scholar]
  12. Birey F, Andersen J, Makinson CD, Islam S, Wei W et al. 2017. Assembly of functionally integrated human forebrain spheroids. Nature 545:54–59
    [Google Scholar]
  13. Boldog E, Bakken TE, Hodge RD, Novotny M, Aevermann BD et al. 2018. Transcriptomic and morphophysiological evidence for a specialized human cortical GABAergic cell type. Nat. Neurosci. 21:1185–95
    [Google Scholar]
  14. Bortone D, Polleux F. 2009. KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 62:53–71
    [Google Scholar]
  15. Buganim Y, Faddah DA, Cheng AW, Itskovich E, Markoulaki S et al. 2012. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150:1209–22
    [Google Scholar]
  16. Burkhalter A. 2008. Many specialists for suppressing cortical excitation. Front. Neurosci. 2:155–67
    [Google Scholar]
  17. Butler A, Hoffman P, Smibert P, Papalexi E, Satija R 2018. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36:411–20
    [Google Scholar]
  18. Butler AB, Reiner A, Karten HJ 2011. Evolution of the amniote pallium and the origins of mammalian neocortex. Ann. N. Y. Acad. Sci. 1225:14–27
    [Google Scholar]
  19. Butt SJ, Fuccillo M, Nery S, Noctor S, Kriegstein A et al. 2005. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48:591–604
    [Google Scholar]
  20. Butt SJ, Sousa VH, Fuccillo MV, Hjerling-Leffler J, Miyoshi G et al. 2008. The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59:722–32
    [Google Scholar]
  21. Buzsaki G. 2002. Theta oscillations in the hippocampus. Neuron 33:325–40
    [Google Scholar]
  22. Cardin JA. 2018. Inhibitory interneurons regulate temporal precision and correlations in cortical circuits. Trends Neurosci 41:689–700
    [Google Scholar]
  23. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F et al. 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:663–67
    [Google Scholar]
  24. Chevy Q, Kepecs A. 2018. When acetylcholine unlocks feedback inhibition in cortex. Neuron 97:481–84
    [Google Scholar]
  25. Cichon J, Gan WB. 2015. Branch-specific dendritic Ca2+ spikes cause persistent synaptic plasticity. Nature 520:180–85
    [Google Scholar]
  26. Close J, Xu H, De Marco Garcia N, Batista-Brito R, Rossignol E et al. 2012. Satb1 is an activity-modulated transcription factor required for the terminal differentiation and connectivity of medial ganglionic eminence-derived cortical interneurons. J. Neurosci. 32:17690–705
    [Google Scholar]
  27. Cossart R. 2011. The maturation of cortical interneuron diversity: how multiple developmental journeys shape the emergence of proper network function. Curr. Opin. Neurobiol. 21:160–68
    [Google Scholar]
  28. Davis-Dusenbery BN, Williams LA, Klim JR, Eggan K 2014. How to make spinal motor neurons. Development 141:491–501
    [Google Scholar]
  29. De Marco Garcia NV, Karayannis T, Fishell G 2011. Neuronal activity is required for the development of specific cortical interneuron subtypes. Nature 472:351–55
    [Google Scholar]
  30. De Marco Garcia NV, Priya R, Tuncdemir SN, Fishell G, Karayannis T 2015. Sensory inputs control the integration of neurogliaform interneurons into cortical circuits. Nat. Neurosci. 18:393–401
    [Google Scholar]
  31. DeBoer EM, Anderson SA. 2017. Fate determination of cerebral cortical GABAergic interneurons and their derivation from stem cells. Brain Res 1655:277–82
    [Google Scholar]
  32. DeFelipe J, Lopez-Cruz PL, Benavides-Piccione R, Bielza C, Larranaga P et al. 2013. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14:202–16
    [Google Scholar]
  33. Dehorter N, Ciceri G, Bartolini G, Lim L, del Pino I, Marin O 2015. Tuning of fast-spiking interneuron properties by an activity-dependent transcriptional switch. Science 349:1216–20
    [Google Scholar]
  34. Dehorter N, Marichal N, Marin O, Berninger B 2017. Tuning neural circuits by turning the interneuron knob. Curr. Opin. Neurobiol. 42:144–51
    [Google Scholar]
  35. Denaxa M, Kalaitzidou M, Garefalaki A, Achimastou A, Lasrado R et al. 2012. Maturation-promoting activity of SATB1 in MGE-derived cortical interneurons. Cell Rep 2:1351–62
    [Google Scholar]
  36. Denaxa M, Neves G, Rabinowitz A, Kemlo S, Liodis P et al. 2018. Modulation of apoptosis controls inhibitory interneuron number in the cortex. Cell Rep 22:1710–21
    [Google Scholar]
  37. Deneris ES, Hobert O. 2014. Maintenance of postmitotic neuronal cell identity. Nat. Neurosci. 17:899–907
    [Google Scholar]
  38. Donato F, Chowdhury A, Lahr M, Caroni P 2015. Early- and late-born parvalbumin basket cell subpopulations exhibiting distinct regulation and roles in learning. Neuron 85:770–86
    [Google Scholar]
  39. Donato F, Rompani SB, Caroni P 2013. Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 504:272–76
    [Google Scholar]
  40. Eiraku M, Watanabe K, Matsuo-Takasaki M, Kawada M, Yonemura S et al. 2008. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3:519–32
    [Google Scholar]
  41. Fairen A. 2007. Cajal and Lorente de Nó on cortical interneurons: coincidences and progress. Brain Res. Rev. 55:430–44
    [Google Scholar]
  42. Favuzzi E, Deogracias R, Marques-Smith A, Maeso P, Jezequel J et al. 2019. Distinct molecular programs regulate synapse specificity in cortical inhibitory circuits. Science 363:413–17
    [Google Scholar]
  43. Feldmeyer D, Qi G, Emmenegger V, Staiger JF 2018. Inhibitory interneurons and their circuit motifs in the many layers of the barrel cortex. Neuroscience 368:132–51
    [Google Scholar]
  44. Ferezou I, Haiss F, Gentet LJ, Aronoff R, Weber B, Petersen CC 2007. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56:907–23
    [Google Scholar]
  45. Fishell G, Rudy B. 2011. Mechanisms of inhibition within the telencephalon: “where the wild things are.”. Annu. Rev. Neurosci. 34:535–67
    [Google Scholar]
  46. Flames N, Pla R, Gelman DM, Rubenstein JL, Puelles L, Marin O 2007. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci. 27:9682–95
    [Google Scholar]
  47. Fogarty M, Grist M, Gelman D, Marin O, Pachnis V, Kessaris N 2007. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27:10935–46
    [Google Scholar]
  48. Fragkouli A, van Wijk NV, Lopes R, Kessaris N, Pachnis V 2009. LIM homeodomain transcription factor-dependent specification of bipotential MGE progenitors into cholinergic and GABAergic striatal interneurons. Development 136:3841–51
    [Google Scholar]
  49. Freund TF. 2003. Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489–95
    [Google Scholar]
  50. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6:347–470
    [Google Scholar]
  51. Froemke RC. 2015. Plasticity of cortical excitatory-inhibitory balance. Annu. Rev. Neurosci. 38:195–219
    [Google Scholar]
  52. Frotscher M. 1998. Cajal-Retzius cells, Reelin, and the formation of layers. Curr. Opin. Neurobiol. 8:570–75
    [Google Scholar]
  53. Fu Y, Tucciarone JM, Espinosa JS, Sheng N, Darcy DP et al. 2014. A cortical circuit for gain control by behavioral state. Cell 156:1139–52
    [Google Scholar]
  54. Furlanis E, Traunmüller L, Fucile G, Scheiffele P 2019. Landscape of ribosome-engaged transcript isoforms reveals extensive neuronal-cell-class-specific alternative splicing programs. Nat. Neurosci 22:1709–17
    [Google Scholar]
  55. Gelman DM, Marin O, Rubenstein JLR 2012. The generation of cortical interneurons. Jasper's Basic Mechanisms of the Epilepsies JL Noebels, M Avoli, MA Rogawski, RW Olsen, AV Delgado-Escueta 786–96 Bethesda, MD: Nat. Cent. Biotechnol. Inf., 4th ed..
    [Google Scholar]
  56. Gelman DM, Martini FJ, Nobrega-Pereira S, Pierani A, Kessaris N, Marin O 2009. The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J. Neurosci. 29:9380–89
    [Google Scholar]
  57. Gentet LJ, Kremer Y, Taniguchi H, Huang ZJ, Staiger JF, Petersen CC 2012. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15:607–12
    [Google Scholar]
  58. Gulyas AI, Hajos N, Freund TF 1996. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J. Neurosci. 16:3397–411
    [Google Scholar]
  59. Haider B, Duque A, Hasenstaub AR, McCormick DA 2006. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J. Neurosci. 26:4535–45
    [Google Scholar]
  60. Hangya B, Pi HJ, Kvitsiani D, Ranade SP, Kepecs A 2014. From circuit motifs to computations: mapping the behavioral repertoire of cortical interneurons. Curr. Opin. Neurobiol. 26:117–24
    [Google Scholar]
  61. Hangya B, Ranade SP, Lorenc M, Kepecs A 2015. Central cholinergic neurons are rapidly recruited by reinforcement feedback. Cell 162:1155–68
    [Google Scholar]
  62. Harris KD, Mrsic-Flogel TD. 2013. Cortical connectivity and sensory coding. Nature 503:51–58
    [Google Scholar]
  63. Harwell CC, Fuentealba LC, Gonzalez-Cerrillo A, Parker PR, Gertz CC et al. 2015. Wide dispersion and diversity of clonally related inhibitory interneurons. Neuron 87:5999–1007
    [Google Scholar]
  64. Hippenmeyer S, Huber RM, Ladle DR, Murphy K, Arber S 2007. ETS transcription factor Erm controls subsynaptic gene expression in skeletal muscles. Neuron 55:726–40
    [Google Scholar]
  65. Hobert O. 2016. Terminal selectors of neuronal identity. Curr. Top. Dev. Biol. 116:455–75
    [Google Scholar]
  66. Hodge RD, Bakken E, Miller JA, Smith KA, Barkan ER et al. 2018. Conserved cell types with divergent features between human and mouse cortex. bioRxiv 384826. https://doi.org/10.1101/384826
    [Crossref]
  67. Hong EJ, McCord AE, Greenberg ME 2008. A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron 60:610–24
    [Google Scholar]
  68. Hopfield JJ. 1982. Neural networks and physical systems with emergent collective computational abilities. PNAS 79:2554–58
    [Google Scholar]
  69. Huang S, Ernberg I, Kauffman S 2009. Cancer attractors: a systems view of tumors from a gene network dynamics and developmental perspective. Semin. Cell Dev. Biol. 20:869–76
    [Google Scholar]
  70. Ibrahim LA, Mesik L, Ji XY, Fang Q, Li HFet al. 2016. Cross-modality sharpening of visual cortical processing through layer-1-mediated inhibition and disinhibition. Neuron 89:1031–45
    [Google Scholar]
  71. Jinno S, Klausberger T, Marton LF, Dalezios Y, Roberts JD et al. 2007. Neuronal diversity in GABAergic long-range projections from the hippocampus. J. Neurosci. 27:8790–804
    [Google Scholar]
  72. Jung H, Mazzoni EO, Soshnikova N, Hanley O, Venkatesh B et al. 2014. Evolving Hox activity profiles govern diversity in locomotor systems. Dev. Cell 29:171–87
    [Google Scholar]
  73. Kanold PO, Luhmann HJ. 2010. The subplate and early cortical circuits. Annu. Rev. Neurosci. 33:23–48
    [Google Scholar]
  74. Karnani MM, Agetsuma M, Yuste R 2014. A blanket of inhibition: functional inferences from dense inhibitory connectivity. Curr. Opin. Neurobiol. 26:96–102
    [Google Scholar]
  75. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7:476–86
    [Google Scholar]
  76. Kelava I, Lewitus E, Huttner WB 2013. The secondary loss of gyrencephaly as an example of evolutionary phenotypical reversal. Front. Neuroanat. 7:16
    [Google Scholar]
  77. Kepecs A, Fishell G. 2014. Interneuron cell types are fit to function. Nature 505:318–26
    [Google Scholar]
  78. Khan AG, Poort J, Chadwick A, Blot A, Sahani M et al. 2018. Distinct learning-induced changes in stimulus selectivity and interactions of GABAergic interneuron classes in visual cortex. Nat. Neurosci. 21:851–59
    [Google Scholar]
  79. Kim D, Jeong H, Lee J, Ghim JW, Her ES et al. 2016. Distinct roles of parvalbumin- and somatostatin-expressing interneurons in working memory. Neuron 92:902–15
    [Google Scholar]
  80. Kim Y, Yang GR, Pradhan K, Venkataraju KU, Bota M et al. 2017. Brain-wide maps reveal stereotyped cell-type-based cortical architecture and subcortical sexual dimorphism. Cell 171:456–69.e22
    [Google Scholar]
  81. Kirschner D, Tsygvintsev A. 2009. On the global dynamics of a model for tumor immunotherapy. Math. Biosci. Eng. 6:573–83
    [Google Scholar]
  82. Klausberger T, Somogyi P. 2008. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53–57
    [Google Scholar]
  83. Koulakov AA, Lazebnik Y. 2012. The problem of colliding networks and its relation to cell fusion and cancer. Biophys. J. 103:2011–20
    [Google Scholar]
  84. Kratsios P, Hobert O. 2018. Nervous system development: flies and worms converging on neuron identity control. Curr. Biol. 28:R1154–57
    [Google Scholar]
  85. Krnjevic K. 1997. Role of GABA in cerebral cortex. Can. J. Physiol. Pharmacol. 75:439–51
    [Google Scholar]
  86. Kubota Y, Kawaguchi Y. 1994. Three classes of GABAergic interneurons in neocortex and neostriatum. Jpn. J. Physiol. 44:Suppl. 2S145–48
    [Google Scholar]
  87. Kvitsiani D, Ranade S, Hangya B, Taniguchi H, Huang JZ, Kepecs A 2013. Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature 498:363–66
    [Google Scholar]
  88. La Manno G, Soldatov R, Zeisel A, Braun E, Hochgerner H et al. 2018. RNA velocity of single cells. Nature 560:494–98
    [Google Scholar]
  89. Laclef C, Metin C. 2018. Conserved rules in embryonic development of cortical interneurons. Semin. Cell Dev. Biol. 76:86–100
    [Google Scholar]
  90. Lagler M, Ozdemir AT, Lagoun S, Malagon-Vina H, Borhegyi Z et al. 2016. Divisions of identified parvalbumin-expressing basket cells during working memory-guided decision making. Neuron 91:1390–401
    [Google Scholar]
  91. Lancaster MA, Renner M, Martin CA, Wenzel D, Bicknell LS et al. 2013. Cerebral organoids model human brain development and microcephaly. Nature 501:373–79
    [Google Scholar]
  92. Lee S, Kruglikov I, Huang ZJ, Fishell G, Rudy B 2013. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat. Neurosci. 16:1662–70
    [Google Scholar]
  93. Lee SH, Kwan AC, Zhang S, Phoumthipphavong V, Flannery JG et al. 2012. Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 488:379–83
    [Google Scholar]
  94. Lee SH, Marchionni I, Bezaire M, Varga C, Danielson N et al. 2014. Parvalbumin-positive basket cells differentiate among hippocampal pyramidal cells. Neuron 82:1129–44
    [Google Scholar]
  95. Letzkus JJ, Wolff SB, Luthi A 2015. Disinhibition, a circuit mechanism for associative learning and memory. Neuron 88:264–76
    [Google Scholar]
  96. Letzkus JJ, Wolff SB, Meyer EM, Tovote P, Courtin J et al. 2011. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480:331–35
    [Google Scholar]
  97. Lewis DA. 2014. Inhibitory neurons in human cortical circuits: substrate for cognitive dysfunction in schizophrenia. Curr. Opin. Neurobiol. 26:22–26
    [Google Scholar]
  98. Lim L, Pakan JMP, Selten MM, Marques-Smith A, Llorca A et al. 2018. Optimization of interneuron function by direct coupling of cell migration and axonal targeting. Nat. Neurosci. 21:920–31
    [Google Scholar]
  99. 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. 27:3078–89
    [Google Scholar]
  100. Litwin-Kumar A, Rosenbaum R, Doiron B 2016. Inhibitory stabilization and visual coding in cortical circuits with multiple interneuron subtypes. J. Neurophysiol. 115:1399–409
    [Google Scholar]
  101. Lodato S, Rouaux C, Quast KB, Jantrachotechatchawan C, Studer M et al. 2011. Excitatory projection neuron subtypes control the distribution of local inhibitory interneurons in the cerebral cortex. Neuron 69:763–79
    [Google Scholar]
  102. Lovett-Barron M, Losonczy A. 2014. Behavioral consequences of GABAergic neuronal diversity. Curr. Opin. Neurobiol. 26:27–33
    [Google Scholar]
  103. Lovett-Barron M, Turi GF, Kaifosh P, Lee PH, Bolze F et al. 2012. Regulation of neuronal input transformations by tunable dendritic inhibition. Nat. Neurosci. 15:423–30
    [Google Scholar]
  104. Lu J, Tucciarone J, Padilla-Coreano N, He M, Gordon JA, Huang ZJ 2017. Selective inhibitory control of pyramidal neuron ensembles and cortical subnetworks by chandelier cells. Nat. Neurosci. 20:1377–83
    [Google Scholar]
  105. Lucas EK, Clem RL. 2018. GABAergic interneurons: the orchestra or the conductor in fear learning and memory?. Brain Res. Bull. 141:13–19
    [Google Scholar]
  106. Luhmann HJ, Khazipov R. 2018. Neuronal activity patterns in the developing barrel cortex. Neuroscience 368:256–67
    [Google Scholar]
  107. Luhmann HJ, Kirischuk S, Sinning A, Kilb W 2014. Early GABAergic circuitry in the cerebral cortex. Curr. Opin. Neurobiol. 26:72–78
    [Google Scholar]
  108. Luo C, Hajkova P, Ecker JR 2018. Dynamic DNA methylation: in the right place at the right time. Science 361:1336–40
    [Google Scholar]
  109. Luo C, Keown CL, Kurihara L, Zhou J, He Y et al. 2017. Single-cell methylomes identify neuronal subtypes and regulatory elements in mammalian cortex. Science 357:600–4
    [Google Scholar]
  110. Maccaferri G, Toth K, McBain CJ 1998. Target-specific expression of presynaptic mossy fiber plasticity. Science 279:1368–70
    [Google Scholar]
  111. Manu Surkova S, Spirov AV, Gursky VV, Janssens H et al. 2009. Canalization of gene expression and domain shifts in the Drosophila blastoderm by dynamical attractors. PLOS Comput. Biol. 5:e1000303
    [Google Scholar]
  112. Mardinly AR, Spiegel I, Patrizi A, Centofante E, Bazinet JE et al. 2016. Sensory experience regulates cortical inhibition by inducing IGF1 in VIP neurons. Nature 531:371–75
    [Google Scholar]
  113. Marin O. 2012. Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13:107–20
    [Google Scholar]
  114. Marin O. 2013. Cellular and molecular mechanisms controlling the migration of neocortical interneurons. Eur. J. Neurosci. 38:2019–29
    [Google Scholar]
  115. Marin O, Rubenstein JL. 2001. A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 2:780–90
    [Google Scholar]
  116. Marin O, Rubenstein JL. 2003. Cell migration in the forebrain. Annu. Rev. Neurosci. 26:441–83
    [Google Scholar]
  117. Mauger O, Lemoine F, Scheiffele P 2016. Targeted intron retention and excision for rapid gene regulation in response to neuronal activity. Neuron 92:1266–78
    [Google Scholar]
  118. Mayer C, Hafemeister C, Bandler RC, Machold R, Batista Brito R et al. 2018. Developmental diversification of cortical inhibitory interneurons. Nature 555:457–62
    [Google Scholar]
  119. Mayer C, Jaglin XH, Cobbs LV, Bandler RC, Streicher C et al. 2015. Clonally related forebrain interneurons disperse broadly across both functional areas and structural boundaries. Neuron 87:5989–98
    [Google Scholar]
  120. McBain CJ, Fisahn A. 2001. Interneurons unbound. Nat. Rev. Neurosci. 2:11–23
    [Google Scholar]
  121. Metin C, Alvarez C, Mondoux D, Vitalis T, Pieau C, Molnár Z 2007. Conserved pattern of tangential neuronal migration during forebrain development. Development 134:2815–27
    [Google Scholar]
  122. Mezger A, Klemm S, Mann I, Brower K, Mir A et al. 2018. High-throughput chromatin accessibility profiling at single-cell resolution. Nat. Commun. 9:3647
    [Google Scholar]
  123. Mi D, Li Z, Lim L, Li M, Moissidis M et al. 2018. Early emergence of cortical interneuron diversity in the mouse embryo. Science 360:81–85
    [Google Scholar]
  124. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF 1996. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815–23
    [Google Scholar]
  125. Miller KD. 2016. Canonical computations of cerebral cortex. Curr. Opin. Neurobiol. 37:75–84
    [Google Scholar]
  126. Minlebaev M, Colonnese M, Tsintsadze T, Sirota A, Khazipov R 2011. Early γ oscillations synchronize developing thalamus and cortex. Science 334:226–29
    [Google Scholar]
  127. Miyoshi G. 2018. Elucidating the developmental trajectories of GABAergic cortical interneuron subtypes. Neurosci. Res. 138:26–32
    [Google Scholar]
  128. Miyoshi G, Butt SJ, Takebayashi H, Fishell G 2007. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J. Neurosci. 27:7786–98
    [Google Scholar]
  129. Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ et al. 2010. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30:1582–94
    [Google Scholar]
  130. Miyoshi G, Young A, Petros T, Karayannis T, McKenzie Chang M et al. 2015. Prox1 regulates the subtype-specific development of caudal ganglionic eminence-derived GABAergic cortical interneurons. J. Neurosci. 35:12869–89
    [Google Scholar]
  131. Moore AK, Wehr M. 2013. Parvalbumin-expressing inhibitory interneurons in auditory cortex are well-tuned for frequency. J. Neurosci. 33:13713–23
    [Google Scholar]
  132. Moore CI, Carlen M, Knoblich U, Cardin JA 2010. Neocortical interneurons: from diversity, strength. Cell 142:189–93
    [Google Scholar]
  133. Munoz W, Tremblay R, Levenstein D, Rudy B 2017. Layer-specific modulation of neocortical dendritic inhibition during active wakefulness. Science 355:954–59
    [Google Scholar]
  134. Naka A, Adesnik H. 2016. Inhibitory circuits in cortical layer 5. Front. Neural Circuits 10:35
    [Google Scholar]
  135. Natan RG, Briguglio JJ, Mwilambwe-Tshilobo L, Jones SI, Aizenberg M, Goldberg EM, Geffen MN 2015. Complementary control of sensory adaptation by two types of cortical interneurons. eLife 4:e09868
    [Google Scholar]
  136. Nery S, Fishell G, Corbin JG 2002. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat. Neurosci. 5:1279–87
    [Google Scholar]
  137. Nguyen TM, Schreiner D, Xiao L, Traunmuller L, Bornmann C, Scheiffele P 2016. An alternative splicing switch shapes neurexin repertoires in principal neurons versus interneurons in the mouse hippocampus. eLife 5:e22757
    [Google Scholar]
  138. Nienborg H, Hasenstaub A, Nauhaus I, Taniguchi H, Huang ZJ, Callaway EM 2013. Contrast dependence and differential contributions from somatostatin- and parvalbumin-expressing neurons to spatial integration in mouse V1. J. Neurosci. 33:11145–54
    [Google Scholar]
  139. Nord AS, Pattabiraman K, Visel A, Rubenstein JLR 2015. Genomic perspectives of transcriptional regulation in forebrain development. Neuron 85:27–47
    [Google Scholar]
  140. Okun M, Lampl I. 2008. Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat. Neurosci. 11:535–37
    [Google Scholar]
  141. Palmer LM, Schulz JM, Murphy SC, Ledergerber D, Murayama M, Larkum ME 2012. The cellular basis of GABAB-mediated interhemispheric inhibition. Science 335:989–93
    [Google Scholar]
  142. Panman L, Andersson E, Alekseenko Z, Hedlund E, Kee N et al. 2011. Transcription factor-induced lineage selection of stem-cell-derived neural progenitor cells. Cell Stem Cell 8:663–75
    [Google Scholar]
  143. Patel T, Hobert O. 2017. Coordinated control of terminal differentiation and restriction of cellular plasticity. eLife 6:e24100
    [Google Scholar]
  144. Paul A, Crow M, Raudales R, He M, Gillis J, Huang ZJ 2017. Transcriptional architecture of synaptic communication delineates GABAergic neuron identity. Cell 171:522–39.e20
    [Google Scholar]
  145. Pelkey KA, Chittajallu R, Craig MT, Tricoire L, Wester JC, McBain CJ 2017. Hippocampal GABAergic inhibitory interneurons. Physiol. Rev. 97:1619–747
    [Google Scholar]
  146. Petilla Interneuron Nomenclature Group 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9:557–68
    [Google Scholar]
  147. Petros TJ, Maurer CW, Anderson SA 2013. Enhanced derivation of mouse ESC-derived cortical interneurons by expression of Nkx2.1. Stem. Cell Res. 11:647–56
    [Google Scholar]
  148. 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. 16:1068–76
    [Google Scholar]
  149. Pi HJ, Hangya B, Kvitsiani D, Sanders JI, Huang ZJ, Kepecs A 2013. Cortical interneurons that specialize in disinhibitory control. Nature 503:521–24
    [Google Scholar]
  150. Pla R, Borrell V, Flames N, Marin O 2006. Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J. Neurosci. 26:6924–34
    [Google Scholar]
  151. Poorthuis RB, Muhammad K, Wang M, Verhoog MB, Junek S et al. 2018. Rapid neuromodulation of layer 1 interneurons in human neocortex. Cell Rep 23:951–58
    [Google Scholar]
  152. Priya R, Paredes MF, Karayannis T, Yusuf N, Liu X et al. 2018. Activity regulates cell death within cortical interneurons through a calcineurin-dependent mechanism. Cell Rep 22:1695–709
    [Google Scholar]
  153. Puelles L. 2017. Comments on the updated tetrapartite pallium model in the mouse and chick, featuring a homologous claustro-insular complex. Brain Behav. Evol. 90:171–89
    [Google Scholar]
  154. Quadrato G, Nguyen T, Macosko EZ, Sherwood JL, Min Yang S et al. 2017. Cell diversity and network dynamics in photosensitive human brain organoids. Nature 545:48–53
    [Google Scholar]
  155. Quattrocolo G, Fishell G, Petros TJ 2017. Heterotopic transplantations reveal environmental influences on interneuron diversity and maturation. Cell Rep 21:721–31
    [Google Scholar]
  156. Quattrocolo G, Maccaferri G. 2013. Novel GABAergic circuits mediating excitation/inhibition of Cajal-Retzius cells in the developing hippocampus. J. Neurosci. 33:5486–98
    [Google Scholar]
  157. Ramón y Cajal S. 1966. Recollections of My Life Cambridge, MA: MIT Press
  158. Roux L, Buzsaki G. 2015. Tasks for inhibitory interneurons in intact brain circuits. Neuropharmacology 88:10–23
    [Google Scholar]
  159. Royer S, Zemelman BV, Losonczy A, Kim J, Chance F et al. 2012. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat. Neurosci. 15:769–75
    [Google Scholar]
  160. Rubenstein JL, Puelles L. 1994. Homeobox gene expression during development of the vertebrate brain. Curr. Top. Dev. Biol. 29:1–63
    [Google Scholar]
  161. Rubin AN, Kessaris N. 2013. PROX1: a lineage tracer for cortical interneurons originating in the lateral/caudal ganglionic eminence and preoptic area. PLOS ONE 8:e77339
    [Google Scholar]
  162. 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
    [Google Scholar]
  163. Saunders A, Macosko EZ, Wysoker A, Goldman M, Krienen FM et al. 2018. Molecular diversity and specializations among the cells of the adult mouse brain. Cell 174:1015–30.e16
    [Google Scholar]
  164. Scala F, Kobak D, Shan S, Bernaerts Y, Laturnus S et al. 2019. Neocortical layer 4 in adult mouse differs in major cell types and circuit organization between primary sensory areas. bioRxiv 507293. https://doi.org/10.1101/507293
    [Crossref]
  165. Schiebinger G, Shu J, Tabaka M, Cleary B, Subramanian V et al. 2019. Optimal-transport analysis of single-cell gene expression identifies developmental trajectories in reprogramming. Cell 176:928–43.e22
    [Google Scholar]
  166. Schreiner D, Nguyen TM, Russo G, Heber S, Patrignani A et al. 2014. Targeted combinatorial alternative splicing generates brain region-specific repertoires of neurexins. Neuron 84:386–98
    [Google Scholar]
  167. Shimamura K, Hartigan DJ, Martinez S, Puelles L, Rubenstein JL 1995. Longitudinal organization of the anterior neural plate and neural tube. Development 121:3923–33
    [Google Scholar]
  168. Shu J, Wu C, Wu Y, Li Z, Shao S et al. 2013. Induction of pluripotency in mouse somatic cells with lineage specifiers. Cell 153:963–75
    [Google Scholar]
  169. Silberberg SN, Taher L, Lindtner S, Sandberg M, Nord AS et al. 2016. Subpallial enhancer transgenic lines: a data and tool resource to study transcriptional regulation of GABAergic cell fate. Neuron 92:59–74
    [Google Scholar]
  170. Skene NG, Bryois J, Bakken TE, Breen G, Crowley JJ et al. 2018. Genetic identification of brain cell types underlying schizophrenia. Nat. Genet. 50:825–33
    [Google Scholar]
  171. Slack JM. 2002. Conrad Hal Waddington: the last Renaissance biologist?. Nat. Rev. Genet. 3:889–95
    [Google Scholar]
  172. Sohal VS, Zhang F, Yizhar O, Deisseroth K 2009. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:698–702
    [Google Scholar]
  173. Somogyi P. 1977. A specific ‘axo-axonal’ interneuron in the visual cortex of the rat. Brain Res 136:345–50
    [Google Scholar]
  174. Spiegel I, Mardinly AR, Gabel HW, Bazinet JE, Couch CH et al. 2014. Npas4 regulates excitatory-inhibitory balance within neural circuits through cell-type-specific gene programs. Cell 157:1216–29
    [Google Scholar]
  175. Spruston N. 2008. Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 9:206–21
    [Google Scholar]
  176. Stokes CC, Teeter CM, Isaacson JS 2014. Single dendrite-targeting interneurons generate branch-specific inhibition. Front. Neural Circuits 8:139
    [Google Scholar]
  177. Striedter GF. 1997. The telencephalon of tetrapods in evolution. Brain Behav. Evol. 49:179–213
    [Google Scholar]
  178. Striedter GF. 2016. Evolution of the hippocampus in reptiles and birds. J. Comp. Neurol. 524:496–517
    [Google Scholar]
  179. Sussel L, Marin O, Kimura S, Rubenstein JL 1999. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126:3359–70
    [Google Scholar]
  180. Szentagothai J. 1975. The ‘module-concept’ in cerebral cortex architecture. Brain Res 95:475–96
    [Google Scholar]
  181. Takada N, Pi HJ, Sousa VH, Waters J, Fishell G et al. 2014. A developmental cell-type switch in cortical interneurons leads to a selective defect in cortical oscillations. Nat. Commun. 5:5333
    [Google Scholar]
  182. Tamamaki N, Tomioka R. 2010. Long-range GABAergic connections distributed throughout the neocortex and their possible function. Front. Neurosci. 4:202
    [Google Scholar]
  183. Tan X, Liu WA, Zhang XJ, Shi W, Ren SQ et al. 2016. Vascular influence on ventral telencephalic progenitors and neocortical interneuron production. Dev. Cell 36:624–38
    [Google Scholar]
  184. Taniguchi H, He M, Wu P, Kim S, Paik R et al. 2011. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71:995–1013
    [Google Scholar]
  185. Taniguchi H, Lu J, Huang ZJ 2013. The spatial and temporal origin of chandelier cells in mouse neocortex. Science 339:70–74
    [Google Scholar]
  186. Tasic B, Menon V, Nguyen TN, Kim TK, Jarsky T et al. 2016. Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat. Neurosci. 19:335–46
    [Google Scholar]
  187. Tasic B, Yao Z, Graybuck LT, Smith KA, Nguyen TN et al. 2018. Shared and distinct transcriptomic cell types across neocortical areas. Nature 563:72–78
    [Google Scholar]
  188. Thion MS, Ginhoux F, Garel S 2018. Microglia and early brain development: an intimate journey. Science 362:185–89
    [Google Scholar]
  189. Tomassy GS, Berger DR, Chen HH, Kasthuri N, Hayworth KJ et al. 2014. Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 344:319–24
    [Google Scholar]
  190. Tosches MA, Yamawaki TM, Naumann RK, Jacobi AA, Tushev G, Laurent G 2018. Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science 360:881–88
    [Google Scholar]
  191. Trapnell C. 2015. Defining cell types and states with single-cell genomics. Genome Res 25:1491–98
    [Google Scholar]
  192. Tsunemoto R, Lee S, Szucs A, Chubukov P, Sokolova I et al. 2018. Diverse reprogramming codes for neuronal identity. Nature 557:375–80
    [Google Scholar]
  193. Tuncdemir SN, Fishell G, Batista-Brito R 2015. miRNAs are essential for the survival and maturation of cortical interneurons. Cereb. Cortex 25:1842–57
    [Google Scholar]
  194. Tuncdemir SN, Wamsley B, Stam FJ, Osakada F, Goulding M et al. 2016. Early somatostatin interneuron connectivity mediates the maturation of deep layer cortical circuits. Neuron 89:521–35
    [Google Scholar]
  195. Turkheimer FE, Leech R, Expert P, Lord LD, Vernon AC 2015. The brain's code and its canonical computational motifs. From sensory cortex to the default mode network: a multi-scale model of brain function in health and disease. Neurosci. Biobehav. Rev. 55:211–22
    [Google Scholar]
  196. Urban-Ciecko J, Barth AL. 2016. Somatostatin-expressing neurons in cortical networks. Nat. Rev. Neurosci. 17:401–9
    [Google Scholar]
  197. Urban-Ciecko J, Jouhanneau JS, Myal SE, Poulet JFA, Barth AL 2018. Precisely timed nicotinic activation drives SST inhibition in neocortical circuits. Neuron 97:611–25.e5
    [Google Scholar]
  198. Veit J, Hakim R, Jadi MP, Sejnowski TJ, Adesnik H 2017. Cortical gamma band synchronization through somatostatin interneurons. Nat. Neurosci. 20:951–59
    [Google Scholar]
  199. Wamsley B, Fishell G. 2017. Genetic and activity-dependent mechanisms underlying interneuron diversity. Nat. Rev. Neurosci. 18:299–309
    [Google Scholar]
  200. Wamsley B, Jaglin XH, Favuzzi E, Quattrocolo G, Nigro MJ et al. 2018. Rbfox1 mediates cell-type-specific splicing in cortical interneurons. Neuron 100:846–59.e7
    [Google Scholar]
  201. Wang DD, Kriegstein AR. 2009. Defining the role of GABA in cortical development. J. Physiol. 587:1873–79
    [Google Scholar]
  202. Webster JC, Mahadevan V, Rhodes CT, Calvigioni D, Venkatesh S, Maric D, Hunt S, Yuan XQ, Zhang Y, Petros TJ, McBain CJ 2019. Neocortical projection neurons instruct inhibitory interneuron circuit development in a lineage-dependent manner. Neuron 102:1–16
    [Google Scholar]
  203. Wehr M, Zador AM. 2003. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442–46
    [Google Scholar]
  204. Wichterle H, Lieberam I, Porter JA, Jessell TM 2002. Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385–97
    [Google Scholar]
  205. Wichterle H, Turnbull DH, 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 128:3759–71
    [Google Scholar]
  206. Wilson NR, Runyan CA, Wang FL, Sur M 2012. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488:343–48
    [Google Scholar]
  207. Wonders CP, Anderson SA. 2006. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 7:687–96
    [Google Scholar]
  208. Wong FK, Bercsenyi K, Sreenivasan V, Portales A, Fernandez-Otero M, Marin O 2018. Pyramidal cell regulation of interneuron survival sculpts cortical networks. Nature 557:668–73
    [Google Scholar]
  209. Wood KC, Blackwell JM, Geffen MN 2017. Cortical inhibitory interneurons control sensory processing. Curr. Opin. Neurobiol. 46:200–7
    [Google Scholar]
  210. Woodruff AR, Anderson SA, Yuste R 2010. The enigmatic function of chandelier cells. Front. Neurosci. 4:201
    [Google Scholar]
  211. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA 2004. Origins of cortical interneuron subtypes. J. Neurosci. 24:2612–22
    [Google Scholar]
  212. Yamanaka S. 2008. Induction of pluripotent stem cells from mouse fibroblasts by four transcription factors. Cell Prolif 41:Suppl. 151–56
    [Google Scholar]
  213. Yang N, Chanda S, Marro S, Ng YH, Janas JA et al. 2017. Generation of pure GABAergic neurons by transcription factor programming. Nat. Methods 14:621–28
    [Google Scholar]
  214. Yavorska I, Wehr M. 2016. Somatostatin-expressing inhibitory interneurons in cortical circuits. Front. Neural Circuits 10:76
    [Google Scholar]
  215. Yoshimura Y, Callaway EM. 2005. Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat. Neurosci. 8:1552–59
    [Google Scholar]
  216. Zeisel A, Hochgerner H, Lonnerberg P, Johnsson A, Memic F et al. 2018. Molecular architecture of the mouse nervous system. Cell 174:999–1014.e22
    [Google Scholar]
  217. Zeisel A, Munoz-Manchado AB, Codeluppi S, Lonnerberg P, La Manno G et al. 2015. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347:1138–42
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-070918-050421
Loading
/content/journals/10.1146/annurev-neuro-070918-050421
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error