1932

Abstract

The neocortex is the part of the brain responsible for execution of higher-order brain functions, including cognition, sensory perception, and sophisticated motor control. During evolution, the neocortex has developed an unparalleled neuronal diversity, which still remains partly unclassified and unmapped at the functional level. Here, we broadly review the structural blueprint of the neocortex and discuss the current classification of its neuronal diversity. We then cover the principles and mechanisms that build neuronal diversity during cortical development and consider the impact of neuronal class-specific identity in shaping cortical connectivity and function.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100814-125353
2015-11-13
2024-04-15
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/31/1/annurev-cellbio-100814-125353.html?itemId=/content/journals/10.1146/annurev-cellbio-100814-125353&mimeType=html&fmt=ahah

Literature Cited

  1. Aboitiz F, Morales D, Montiel J. 2003. The evolutionary origin of the mammalian isocortex: towards an integrated developmental and functional approach. Behav. Brain Sci. 26:5535–52; discussion 552–85 [Google Scholar]
  2. Alcamo EA, Chirivella L, Dautzenberg M, Dobreva G, Farinas I. et al. 2008. Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57:3364–77 [Google Scholar]
  3. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL. 1997. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:5337474–76 [Google Scholar]
  4. Angevine JBJ, Sidman RL. 1961. Autoradiographic study of cell migration during histogenesis of cerebral cortex in mouse. Nature 192:766–68 [Google Scholar]
  5. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD. 2005. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45:2207–21 [Google Scholar]
  6. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R. et al. 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9:7557–68 [Google Scholar]
  7. Azim E, Jabaudon D, Fame RM, Macklis JD. 2009. SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development. Nat. Neurosci. 12:101238–47 [Google Scholar]
  8. Baranek C, Dittrich M, Parthasarathy S, Bonnon CG, Britanova O. et al. 2012. Protooncogene Ski cooperates with the chromatin-remodeling factor Satb2 in specifying callosal neurons. PNAS 109:93546–51 [Google Scholar]
  9. 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 63:4466–81 [Google Scholar]
  10. Bayer SA, Altman J. 1991. Neocortical Development New York: Raven
  11. Berry M, Rogers AW. 1965. The migration of neuroblasts in the developing cerebral cortex. J. Anat. 99:4691–709 [Google Scholar]
  12. Britanova O, de Juan Romero C, Cheung A, Kwan KY, Schwark M. et al. 2008. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57:3378–92 [Google Scholar]
  13. Broca P. 1865. Sur le siège de la faculté du langage articulé. Bull. Soc. Anthropol. Paris 6:337–93 [Google Scholar]
  14. Brown KN, Chen S, Han Z, Lu C-H, Tan X. et al. 2011. Clonal production and organization of inhibitory interneurons in the neocortex. Science 334:6055480–86 [Google Scholar]
  15. Brown SP, Hestrin S. 2009. Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457:72331133–36 [Google Scholar]
  16. 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 59:5722–32 [Google Scholar]
  17. Bystron I, Blakemore C, Rakic P. 2008. Development of the human cerebral cortex: Boulder Committee revisited. Nat. Rev. Neurosci. 9:2110–22 [Google Scholar]
  18. Calegari F, Haubensak W, Haffner C, Huttner WB. 2005. Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J. Neurosci. 25:286533–38 [Google Scholar]
  19. Calegari F, Huttner WB. 2003. An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J. Cell Sci. 116:Pt. 244947–55 [Google Scholar]
  20. Callaway EM, Luo L. 2015. Monosynaptic circuit tracing with glycoprotein-deleted rabies viruses. J. Neurosci. 35:248979–85 [Google Scholar]
  21. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F. et al. 2010. Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nat. Protoc. 5:2247–54 [Google Scholar]
  22. Catapano LA, Magavi SS, Macklis JD. 2008. Neuroanatomical tracing of neuronal projections with Fluoro-Gold. Methods Mol. Biol. 438:353–59 [Google Scholar]
  23. Caviness VS. 1982. Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res. 256:3293–302 [Google Scholar]
  24. Cederquist GY, Azim E, Shnider SJ, Padmanabhan H, Macklis JD. 2013. Lmo4 establishes rostral motor cortex projection neuron subtype diversity. J. Neurosci. 33:156321–32 [Google Scholar]
  25. Chen F, Tillberg PW, Boyden ES. 2015. Optical imaging. Expansion microscopy. Science 347:6221543–48 [Google Scholar]
  26. Ciceri G, Dehorter N, Sols I, Huang ZJ, Maravall M, Marín O. 2013. Lineage-specific laminar organization of cortical GABAergic interneurons. Nat. Neurosci. 16:91199–210 [Google Scholar]
  27. Close J, Xu H, De Marco García 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. 32:4917690–705 [Google Scholar]
  28. da Costa NM, Martin KAC. 2010. Whose cortical column would that be?. Front. Neuroanat. 4:16 [Google Scholar]
  29. De la Rossa A, Bellone C, Golding B, Vitali I, Moss J. et al. 2013. In vivo reprogramming of circuit connectivity in postmitotic neocortical neurons. Nat. Neurosci. 16:2193–200 [Google Scholar]
  30. 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. 2:51351–62 [Google Scholar]
  31. Desai AR, McConnell SK. 2000. Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127:132863–72 [Google Scholar]
  32. Dugas JC, Mandemakers W, Rogers M, Ibrahim A, Daneman R, Barres BA. 2008. A novel purification method for CNS projection neurons leads to the identification of brain vascular cells as a source of trophic support for corticospinal motor neurons. J. Neurosci. 28:338294–305 [Google Scholar]
  33. Eckler MJ, Nguyen TD, McKenna WL, Fastow BL, Guo C. et al. 2015. Cux2-positive radial glial cells generate diverse subtypes of neocortical projection neurons and macroglia. Neuron 86:41100–8 [Google Scholar]
  34. Fietz SA, Huttner WB. 2011. Cortical progenitor expansion, self-renewal and neurogenesis—a polarized perspective. Curr. Opin. Neurobiol. 21:123–35 [Google Scholar]
  35. Fino E, Yuste R. 2011. Dense inhibitory connectivity in neocortex. Neuron 69:61188–203 [Google Scholar]
  36. Flames N, Pla R, Gelman DM, Rubenstein JLR, Puelles L, Marín O. 2007. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci. 27:369682–95 [Google Scholar]
  37. Fogarty M, Grist M, Gelman DM, Marin O, Pachnis V, Kessaris N. 2007. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27:4110935–46 [Google Scholar]
  38. Franco SJ, Gil-Sanz C, Martinez-Garay I, Espinosa A, Harkins-Perry SR. et al. 2012. Fate-restricted neural progenitors in the mammalian cerebral cortex. Science 337:6095746–49 [Google Scholar]
  39. Frantz GD, McConnell SK. 1996. Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron 17:155–61 [Google Scholar]
  40. Frostig RD. 2006. Functional organization and plasticity in the adult rat barrel cortex: moving out-of-the-box. Curr. Opin. Neurobiol. 16:4445–50 [Google Scholar]
  41. Gao P, Postiglione MP, Krieger TG, Hernandez L, Wang C. et al. 2014. Deterministic progenitor behavior and unitary production of neurons in the neocortex. Cell 159:4775–88 [Google Scholar]
  42. Gelman DM, Griveau A, Dehorter N, Teissier A, Varela C. et al. 2011. A wide diversity of cortical GABAergic interneurons derives from the embryonic preoptic area. J. Neurosci. 31:4616570–80 [Google Scholar]
  43. 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. 29:299380–89 [Google Scholar]
  44. Gil-Sanz C, Espinosa A, Fregoso SP, Bluske KK, Cunningham CL. et al. 2015. Lineage tracing using Cux2-Cre and Cux2-CreERT2 mice. Neuron 86:41091–99 [Google Scholar]
  45. Greig LC, Woodworth MB, Galazo MJ, Padmanabhan H, Macklis JD. 2013. Molecular logic of neocortical projection neuron specification, development and diversity. Nat. Rev. Neurosci. 14:11755–69 [Google Scholar]
  46. Guo C, Eckler MJ, McKenna WL, McKinsey GL, Rubenstein JLR, Chen B. 2013. Fezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes. Neuron 80:51167–74 [Google Scholar]
  47. Guo J, Anton ES. 2014. Decision making during interneuron migration in the developing cerebral cortex. Trends Cell Biol. 24:6342–51 [Google Scholar]
  48. Han W, Kwan KY, Shim S, Lam MMS, Shin Y. et al. 2011. TBR1 directly represses Fezf2 to control the laminar origin and development of the corticospinal tract. PNAS 108:73041–46 [Google Scholar]
  49. Hansen DV, Lui JH, Parker PRL, Kriegstein AR. 2010. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:7288554–61 [Google Scholar]
  50. Haubensak W, Attardo A, Denk W, Huttner WB. 2004. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. PNAS 101:93196–201 [Google Scholar]
  51. Huang ZJ, Zeng H. 2013. Genetic approaches to neural circuits in the mouse. Annu. Rev. Neurosci. 36:183–215 [Google Scholar]
  52. Johnson MB, Wang PP, Atabay KD, Murphy EA, Doan RN. et al. 2015. Single-cell analysis reveals transcriptional heterogeneity of neural progenitors in human cortex. Nat. Neurosci. 18:5637–46 [Google Scholar]
  53. Joshi PS, Molyneaux BJ, Feng L, Xie X, Macklis JD, Gan L. 2008. Bhlhb5 regulates the postmitotic acquisition of area identities in layers II–V of the developing neocortex. Neuron 60:2258–72 [Google Scholar]
  54. Kepecs A, Fishell G. 2014. Interneuron cell types are fit to function. Nature 505:7483318–26 [Google Scholar]
  55. Kohwi M, Doe CQ. 2013. Temporal fate specification and neural progenitor competence during development. Nat. Rev. Neurosci. 14:12823–38 [Google Scholar]
  56. Kowalczyk T, Pontious A, Englund C, Daza RAM, Bedogni F. et al. 2009. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex 19:102439–50 [Google Scholar]
  57. Lai T, Jabaudon D, Molyneaux BJ, Azim E, Arlotta P. et al. 2008. SOX5 controls the sequential generation of distinct corticofugal neuron subtypes. Neuron 57:2232–47 [Google Scholar]
  58. LaVail JH, Winston KR, Tish A. 1973. A method based on retrograde intraaxonal transport of protein for identification of cell bodies of origin of axons terminating within the CNS. Brain Res. 58:2470–77 [Google Scholar]
  59. Lee AT, Gee SM, Vogt D, Patel T, Rubenstein JL, Sohal VS. 2014. Pyramidal neurons in prefrontal cortex receive subtype-specific forms of excitation and inhibition. Neuron 81:161–68 [Google Scholar]
  60. Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B. 2010. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J. Neurosci. 30:5016796–808 [Google Scholar]
  61. Lee S, Kruglikov I, Huang ZJ, Fishell G, Rudy B. 2013. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat. Neurosci. 16:111662–70 [Google Scholar]
  62. 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. 27:123078–89 [Google Scholar]
  63. Lodato S, Molyneaux BJ, Zuccaro E, Goff LA, Chen H-H. et al. 2014a. Gene co-regulation by Fezf2 selects neurotransmitter identity and connectivity of corticospinal neurons. Nat. Neurosci. 17:81046–54 [Google Scholar]
  64. 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 69:4763–79 [Google Scholar]
  65. Lodato S, Shetty AS, Arlotta P. 2014b. Cerebral cortex assembly: generating and reprogramming projection neuron diversity. Trends Neurosci. 38:2117–25 [Google Scholar]
  66. Luskin MB, Pearlman AL, Sanes JR. 1988. Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1:8635–47 [Google Scholar]
  67. Malatesta P, Hartfuss E, Götz M. 2000. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127:245253–63 [Google Scholar]
  68. Marín O, Noebels JL, Avoli M, Rogawski MA, Olsen RW. et al. 2012. The generation of cortical interneurons. Nat. Rev. Neurosci. 13:2107–20 [Google Scholar]
  69. Markram H. 2006. The Blue Brain Project. Nat. Rev. Neurosci. 7:2153–60 [Google Scholar]
  70. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5:10793–807 [Google Scholar]
  71. McConnell SK, Kaznowski CE. 1991. Cell cycle dependence of laminar determination in developing neocortex. Science 254:5029282–85 [Google Scholar]
  72. McKenna WL, Betancourt J, Larkin KA, Abrams B, Guo C. et al. 2011. Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J. Neurosci. 31:2549–64 [Google Scholar]
  73. Miyata T, Kawaguchi A, Okano H, Ogawa M. 2001. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:5727–41 [Google Scholar]
  74. Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJB. et al. 2010. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30:51582–94 [Google Scholar]
  75. Molyneaux BJ, Arlotta P, Fame RM, MacDonald JL, MacQuarrie KL, Macklis JD. 2009. Novel subtype-specific genes identify distinct subpopulations of callosal projection neurons. J. Neurosci. 29:3912343–54 [Google Scholar]
  76. Molyneaux BJ, Arlotta P, Menezes JRL, Macklis JD. 2007. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8:6427–37 [Google Scholar]
  77. Molyneaux BJ, Goff LA, Brettler AC, Chen H-H, Brown JR. et al. 2015. DeCoN: genome-wide analysis of in vivo transcriptional dynamics during pyramidal neuron fate selection in neocortex. Neuron 85:2275–88 [Google Scholar]
  78. Morishima M, Morita K, Kubota Y, Kawaguchi Y. 2011. Highly differentiated projection-specific cortical subnetworks. J. Neurosci. 31:2810380–91 [Google Scholar]
  79. Mountcastle VB. 1957. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J. Neurophysiol. 20:4408–34 [Google Scholar]
  80. Neves G, Shah MM, Liodis P, Achimastou A, Denaxa M. et al. 2013. The LIM homeodomain protein Lhx6 regulates maturation of interneurons and network excitability in the mammalian cortex. Cereb. Cortex 23:81811–23 [Google Scholar]
  81. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:6821714–20 [Google Scholar]
  82. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7:2136–44 [Google Scholar]
  83. Osakada F, Callaway EM. 2013. Design and generation of recombinant rabies virus vectors. Nat. Protoc. 8:81583–601 [Google Scholar]
  84. Otsuka T, Kawaguchi Y. 2009. Cortical inhibitory cell types differentially form intralaminar and interlaminar subnetworks with excitatory neurons. J. Neurosci. 29:3410533–40 [Google Scholar]
  85. Petersen CC, Sakmann B. 2001. Functionally independent columns of rat somatosensory barrel cortex revealed with voltage-sensitive dye imaging. J. Neurosci. 21:218435–46 [Google Scholar]
  86. Pi H-J, Hangya B, Kvitsiani D, Sanders JI, Huang ZJ, Kepecs A. 2013. Cortical interneurons that specialize in disinhibitory control. Nature 503:7477521–24 [Google Scholar]
  87. Pilaz L-J, Patti D, Marcy G, Ollier E, Pfister S. et al. 2009. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. PNAS 106:5121924–29 [Google Scholar]
  88. Pilz G-A, Shitamukai A, Reillo I, Pacary E, Schwausch J. et al. 2013. Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type. Nat. Commun. 4:2125 [Google Scholar]
  89. Qi Y, Stapp D, Qiu M. 2002. Origin and molecular specification of oligodendrocytes in the telencephalon. Trends Neurosci. 25:5223–25 [Google Scholar]
  90. Ramón y Cajal S. 1909. Histologie du Système Nerveux de l'Homme et des Vértébres. Paris: Maloine
  91. Ramón y Cajal S. 1967 (1906). The structure and connexions of neurons. Nobel Lecture, December 12, 1906. Nobel Lectures Physiology or Medicine 1901–1921220–53 Amsterdam: Elsevier [Google Scholar]
  92. Rash BG, Grove EA. 2006. Area and layer patterning in the developing cerebral cortex. Curr. Opin. Neurobiol. 16:125–34 [Google Scholar]
  93. Renier N, Wu Z, Simon DJ, Yang J, Ariel P, Tessier-Lavigne M. 2014. iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159:4896–910 [Google Scholar]
  94. Rouaux C, Arlotta P. 2013. Direct lineage reprogramming of post-mitotic callosal neurons into corticofugal neurons in vivo. Nat. Cell Biol. 15:2214–21 [Google Scholar]
  95. Rudy B, Fishell G, Lee S, Hjerling-Leffler J. 2011. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71:145–61 [Google Scholar]
  96. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN. et al. 2006. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat. Neurosci. 9:6743–51 [Google Scholar]
  97. Shepherd GMG. 2013. Corticostriatal connectivity and its role in disease. Nat. Rev. Neurosci. 14:4278–91 [Google Scholar]
  98. Sousa VH, Miyoshi G, Hjerling-Leffler J, Karayannis T, Fishell G. 2009. Characterization of Nkx6-2-derived neocortical interneuron lineages. Cereb. Cortex 19:Suppl. 1i1–10 [Google Scholar]
  99. Srinivasan K, Leone DP, Bateson RK, Dobreva G, Kohwi Y. et al. 2012. A network of genetic repression and derepression specifies projection fates in the developing neocortex. PNAS 109:4719071–78 [Google Scholar]
  100. Takahashi T, Nowakowski RS, Caviness VSJ. 1995. Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J. Neurosci. 15:96058–68 [Google Scholar]
  101. Tamamaki N, Fujimori KE, Takauji R. 1997. Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J. Neurosci. 17:218313–23 [Google Scholar]
  102. Taverna E, Götz M, Huttner WB. 2014. The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex. Annu. Rev. Cell Dev. Biol. 30:465–502 [Google Scholar]
  103. Tomassy GS, Berger DR, Chen H-H, Kasthuri N, Hayworth KJ. et al. 2014. Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 344:6181319–24 [Google Scholar]
  104. Varga C, Lee SY, Soltesz I. 2010. Target-selective GABAergic control of entorhinal cortex output. Nat. Neurosci. 13:7822–24 [Google Scholar]
  105. Vasistha NA, García-Moreno F, Arora S, Cheung AFP, Arnold SJ. et al. 2015. Cortical and clonal contribution of Tbr2 expressing progenitors in the developing mouse brain. Cereb. Cortex 25103290–302
  106. Vitalis T, Rossier J. 2011. New insights into cortical interneurons development and classification: contribution of developmental studies. Dev. Neurobiol. 71:134–44 [Google Scholar]
  107. Walsh C, Cepko CL. 1993. Clonal dispersion in proliferative layers of developing cerebral cortex. Nature 362:6421632–35 [Google Scholar]
  108. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA. 2004. Origins of cortical interneuron subtypes. J. Neurosci. 24:112612–22 [Google Scholar]
  109. Xu Q, Tam M, Anderson SA. 2008. Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J. Comp. Neurol. 506:116–29 [Google Scholar]
  110. Yamawaki N, Borges K, Suter BA, Harris KD, Shepherd GMG. 2014. A genuine layer 4 in motor cortex with prototypical synaptic circuit connectivity. eLife 3:e05422 [Google Scholar]
  111. Yoshimura Y, Callaway EM. 2005. Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat. Neurosci. 8:111552–59 [Google Scholar]
  112. Zeisel A, Muñoz-Manchado AB, Codeluppi S, Lönnerberg P, La Manno G. et al. 2015. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347:62261138–42 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100814-125353
Loading
/content/journals/10.1146/annurev-cellbio-100814-125353
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