The neocortical circuit: themes and variations

Subjects

Abstract

Similarities in neocortical circuit organization across areas and species suggest a common strategy to process diverse types of information, including sensation from diverse modalities, motor control and higher cognitive processes. Cortical neurons belong to a small number of main classes. The properties of these classes, including their local and long-range connectivity, developmental history, gene expression, intrinsic physiology and in vivo activity patterns, are remarkably similar across areas. Each class contains subclasses; for a rapidly growing number of these, conserved patterns of input and output connections are also becoming evident. The ensemble of circuit connections constitutes a basic circuit pattern that appears to be repeated across neocortical areas, with area- and species-specific modifications. Such 'serially homologous' organization may adapt individual neocortical regions to the type of information each must process.

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Figure 1: Dendritic morphology of excitatory neurons in S1 barrel cortex.
Figure 2: Excitatory hodology of ECs in layers 2–5, including intratelencephalic neurons in layer 4 (L4 IT), IT neurons of other layers (L2/3, L5A, L5B; grouped as IT here) and pyramidal tract (PT) neurons.
Figure 3: Thalamocortical (TC) input streams.
Figure 4: Hypothesized excitatory hodology of the main EC classes.
Figure 5: Hypothesized homologous hodology of inter-areal connectivity.
Figure 6: Sequential hodology of three main inhibitory cell classes.

References

  1. 1

    Douglas, R.J., Martin, K.A. & Whitteridge, D. A canonical microcircuit for neocortex. Neural Comput. 1, 480–488 (1989).

    Article  Google Scholar 

  2. 2

    Douglas, R.J. & Martin, K.A. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419–451 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 3

    Thomson, A.M. & Lamy, C. Functional maps of neocortical local circuitry. Front. Neurosci. 1, 19–42 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. 4

    Harris, K.D. & Mrsic-Flogel, T.D. Cortical connectivity and sensory coding. Nature 503, 51–58 (2013).

    Article  CAS  Google Scholar 

  5. 5

    Braitenberg, V.B. & Schuz, A. Cortex: Statistics and Geometry of Neuronal Connectivity (Springer, Berlin, 1998).

  6. 6

    Oberlaender, M. et al. Cell type-specific three-dimensional structure of thalamocortical circuits in a column of rat vibrissal cortex. Cereb. Cortex 22, 2375–2391 (2012).

    Article  Google Scholar 

  7. 7

    Stepanyants, A., Martinez, L.M., Ferecsko, A.S. & Kisvarday, Z.F. The fractions of short- and long-range connections in the visual cortex. Proc. Natl. Acad. Sci. USA 106, 3555–3560 (2009).

    Article  Google Scholar 

  8. 8

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

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9

    Ko, H. et al. Functional specificity of local synaptic connections in neocortical networks. Nature 473, 87–91 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Shepherd, G.M.G. Corticostriatal connectivity and its role in disease. Nat. Rev. Neurosci. 14, 278–291 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 11

    Greig, L.C., Woodworth, M.B., Galazo, M.J., Padmanabhan, H. & Macklis, J.D. Molecular logic of neocortical projection neuron specification, development and diversity. Nat. Rev. Neurosci. 14, 755–769 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 12

    Gerfen, C.R., Paletzki, R. & Heintz, N. GENSAT BAC cre-recombinase driver lines to study the functional organization of cerebral cortical and basal ganglia circuits. Neuron 80, 1368–1383 (2013).

    Article  CAS  Google Scholar 

  13. 13

    Huang, Z.J. Toward a genetic dissection of cortical circuits in the mouse. Neuron 83, 1284–1302 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

    von Economo, C. The Cytoarchitectonics of the Human Cerebral Cortex (Oxford Univ. Press, London, 1929).

  15. 15

    Morishima, M. & Kawaguchi, Y. Recurrent connection patterns of corticostriatal pyramidal cells in frontal cortex. J. Neurosci. 26, 4394–4405 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 16

    Petreanu, L., Mao, T., Sternson, S.M. & Svoboda, K. The subcellular organization of neocortical excitatory connections. Nature 457, 1142–1145 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    Brown, S.P. & Hestrin, S. Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457, 1133–1136 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 18

    Kiritani, T., Wickersham, I.R., Seung, H.S. & Shepherd, G.M.G. Hierarchical connectivity and connection-specific dynamics in the corticospinal-corticostriatal microcircuit in mouse motor cortex. J. Neurosci. 32, 4992–5001 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 19

    Lefort, S., Tomm, C., Floyd Sarria, J.C. & Petersen, C.C. The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 61, 301–316 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 20

    Lorente de No, R. Cerebral cortex: architecture, intracortical connections, motor projections. in Physiology of the Nervous System 3rd edn. (ed. Fulton, J.F.) 288–330 (Oxford Univ. Press, London, 1949).

  21. 21

    Evarts, E.V., Shinoda, Y. & Wise, S.P. Neurophysiological Approaches to Higher Brain Functions (Wiley, New York, 1984).

  22. 22

    Jones, E.G. The thalamic matrix and thalamocortical synchrony. Trends Neurosci. 24, 595–601 (2001).

    Article  CAS  Google Scholar 

  23. 23

    Clascá, F., Rubio-Garrido, P. & Jabaudon, D. Unveiling the diversity of thalamocortical neuron subtypes. Eur. J. Neurosci. 35, 1524–1532 (2012).

    Article  Google Scholar 

  24. 24

    Parent, M. & Parent, A. Single-axon tracing and three-dimensional reconstruction of centre median-parafascicular thalamic neurons in primates. J. Comp. Neurol. 481, 127–144 (2005).

    Article  Google Scholar 

  25. 25

    Wimmer, V.C., Bruno, R.M., de Kock, C.P., Kuner, T. & Sakmann, B. Dimensions of a projection column and architecture of VPM and POm axons in rat vibrissal cortex. Cereb. Cortex 20, 2265–2276 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  26. 26

    Smith, P.H., Uhlrich, D.J., Manning, K.A. & Banks, M.I. Thalamocortical projections to rat auditory cortex from the ventral and dorsal divisions of the medial geniculate nucleus. J. Comp. Neurol. 520, 34–51 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. 27

    Kimura, A., Donishi, T., Sakoda, T., Hazama, M. & Tamai, Y. Auditory thalamic nuclei projections to the temporal cortex in the rat. Neuroscience 117, 1003–1016 (2003).

    Article  CAS  Google Scholar 

  28. 28

    Nassi, J.J. & Callaway, E.M. Parallel processing strategies of the primate visual system. Nat. Rev. Neurosci. 10, 360–372 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

    Herkenham, M. Laminar organization of thalamic projections to the rat neocortex. Science 207, 532–535 (1980).

    Article  CAS  Google Scholar 

  30. 30

    Cruz-Martín, A. et al. A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex. Nature 507, 358–361 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 31

    Kaneko, T. Local connections of excitatory neurons in motor-associated cortical areas of the rat. Front. Neural Circuits 7, 75 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  32. 32

    Hooks, B.M. et al. Laminar organization of long-range excitatory input to mouse motor cortex. J. Neurosci. 33, 748–760 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 33

    Theyel, B.B., Llano, D.A. & Sherman, S.M. The corticothalamocortical circuit drives higher-order cortex in the mouse. Nat. Neurosci. 13, 84–88 (2010).

    Article  CAS  Google Scholar 

  34. 34

    Pouchelon, G. et al. Modality-specific thalamocortical inputs instruct the identity of postsynaptic L4 neurons. Nature 511, 471–474 (2014).

    Article  CAS  Google Scholar 

  35. 35

    Fitzpatrick, D. The functional organization of local circuits in visual cortex: insights from the study of tree shrew striate cortex. Cereb. Cortex 6, 329–341 (1996).

    Article  CAS  Google Scholar 

  36. 36

    Thomson, A.M. Neocortical layer 6, a review. Front. Neuroanat. 4, 13 (2010).

    PubMed  PubMed Central  Google Scholar 

  37. 37

    Weiler, N., Wood, L., Yu, J., Solla, S.A. & Shepherd, G.M.G. Top-down laminar organization of the excitatory network in motor cortex. Nat. Neurosci. 11, 360–366 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 38

    Hooks, B.M. et al. Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas. PLoS Biol. 9, e1000572 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 39

    Schubert, D., Kötter, R., Zilles, K., Luhmann, H.J. & Staiger, J.F. Cell type-specific circuits of cortical layer IV spiny neurons. J. Neurosci. 23, 2961–2970 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 40

    Kim, J., Matney, C.J., Blankenship, A., Hestrin, S. & Brown, S.P. Layer 6 corticothalamic neurons activate a cortical output layer, layer 5a. J. Neurosci. 34, 9656–9664 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 41

    Lee, C.C. & Sherman, S.M. Modulator property of the intrinsic cortical projection from layer 6 to layer 4. Front. Syst. Neurosci. 3, 3 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. 42

    Olsen, S.R., Bortone, D.S., Adesnik, H. & Scanziani, M. Gain control by layer six in cortical circuits of vision. Nature 483, 47–52 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 43

    Staiger, J.F. et al. Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells. Cereb. Cortex 14, 690–701 (2004).

    Article  Google Scholar 

  44. 44

    Peters, A. & Kara, D.A. The neuronal composition of area 17 of rat visual cortex. I. The pyramidal cells. J. Comp. Neurol. 234, 218–241 (1985).

    Article  CAS  Google Scholar 

  45. 45

    Smith, P.H. & Populin, L.C. Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices. J. Comp. Neurol. 436, 508–519 (2001).

    Article  CAS  Google Scholar 

  46. 46

    Zhou, M. et al. Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. Nat. Neurosci. 17, 841–850 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. 47

    Hansen, B.J., Chelaru, M.I. & Dragoi, V. Correlated variability in laminar cortical circuits. Neuron 76, 590–602 (2012).

    Article  CAS  Google Scholar 

  48. 48

    Smith, M.A., Jia, X., Zandvakili, A. & Kohn, A. Laminar dependence of neuronal correlations in visual cortex. J. Neurophysiol. 109, 940–947 (2013).

    Article  Google Scholar 

  49. 49

    Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).

    Article  CAS  Google Scholar 

  50. 50

    Van Hooser, S.D., Roy, A., Rhodes, H.J., Culp, J.H. & Fitzpatrick, D. Transformation of receptive field properties from lateral geniculate nucleus to superficial V1 in the tree shrew. J. Neurosci. 33, 11494–11505 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 51

    Cruikshank, S.J., Lewis, T.J. & Connors, B.W. Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat. Neurosci. 10, 462–468 (2007).

    Article  CAS  Google Scholar 

  52. 52

    Swadlow, H.A. Thalamocortical control of feed-forward inhibition in awake somatosensory 'barrel' cortex. Phil. Trans. R. Soc. Lond. B 357, 1717–1727 (2002).

    Article  Google Scholar 

  53. 53

    Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442–446 (2003).

    Article  CAS  Google Scholar 

  54. 54

    Wilent, W.B. & Contreras, D. Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat. Neurosci. 8, 1364–1370 (2005).

    Article  CAS  Google Scholar 

  55. 55

    Shepherd, G.M.G. Intracortical cartography in an agranular area. Front. Neurosci. 3, 337–343 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  56. 56

    Alfano, C. & Studer, M. Neocortical arealization: evolution, mechanisms, and open questions. Dev. Neurobiol. 73, 411–447 (2013).

    Article  Google Scholar 

  57. 57

    Rowell, J.J., Mallik, A.K., Dugas-Ford, J. & Ragsdale, C.W. Molecular analysis of neocortical layer structure in the ferret. J. Comp. Neurol. 518, 3272–3289 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 58

    García-Cabezas, M.A. & Barbas, H. Area 4 has layer IV in adult primates. Eur. J. Neurosci. 39, 1824–1834 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59

    Coogan, T.A. & Burkhalter, A. Hierarchical organization of areas in rat visual cortex. J. Neurosci. 13, 3749–3772 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. 60

    Rockland, K.S. & Pandya, D.N. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res. 179, 3–20 (1979).

    Article  CAS  Google Scholar 

  61. 61

    Markov, N.T. & Kennedy, H. The importance of being hierarchical. Curr. Opin. Neurobiol. 23, 187–194 (2013).

    Article  CAS  Google Scholar 

  62. 62

    Petreanu, L., Huber, D., Sobczyk, A. & Svoboda, K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10, 663–668 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. 63

    Adesnik, H. & Scanziani, M. Lateral competition for cortical space by layer-specific horizontal circuits. Nature 464, 1155–1160 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. 64

    Sato, T.R. & Svoboda, K. The functional properties of barrel cortex neurons projecting to the primary motor cortex. J. Neurosci. 30, 4256–4260 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. 65

    Chen, J.L., Carta, S., Soldado-Magraner, J., Schneider, B.L. & Helmchen, F. Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex. Nature 499, 336–340 (2013).

    Article  CAS  Google Scholar 

  66. 66

    Yamashita, T. et al. Membrane potential dynamics of neocortical projection neurons driving target-specific signals. Neuron 80, 1477–1490 (2013).

    Article  CAS  Google Scholar 

  67. 67

    Bureau, I., Shepherd, G.M.G. & Svoboda, K. Precise development of functional and anatomical columns in the neocortex. Neuron 42, 789–801 (2004).

    Article  CAS  Google Scholar 

  68. 68

    Staiger, J.F., Bojak, I., Miceli, S. & Schubert, D. A gradual depth-dependent change in connectivity features of supragranular pyramidal cells in rat barrel cortex. Brain Struct. Funct. doi:10.1007/s00429-014-0726-8 (2014).

  69. 69

    Shepherd, G.M.G. & Svoboda, K. Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J. Neurosci. 25, 5670 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. 70

    Anderson, C.T., Sheets, P.L., Kiritani, T. & Shepherd, G.M.G. Sublayer-specific microcircuits of corticospinal and corticostriatal neurons in motor cortex. Nat. Neurosci. 13, 739–744 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. 71

    de Kock, C.P., Bruno, R.M., Spors, H. & Sakmann, B. Layer- and cell-type-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J. Physiol. (Lond.) 581, 139–154 (2007).

    Article  CAS  Google Scholar 

  72. 72

    Sakata, S. & Harris, K.D. Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 64, 404–418 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. 73

    Niell, C.M. & Stryker, M.P. Highly selective receptive fields in mouse visual cortex. J. Neurosci. 28, 7520–7536 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 74

    Hromádka, T., Deweese, M.R. & Zador, A.M. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol. 6, e16 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. 75

    O'Connor, D.H., Peron, S.P., Huber, D. & Svoboda, K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67, 1048–1061 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. 76

    Helmstaedter, M., Staiger, J.F., Sakmann, B. & Feldmeyer, D. Efficient recruitment of layer 2/3 interneurons by layer 4 input in single columns of rat somatosensory cortex. J. Neurosci. 28, 8273–8284 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. 77

    Diamond, M.E., Huang, W. & Ebner, F.F. Laminar comparison of somatosensory cortical plasticity. Science 265, 1885–1888 (1994).

    Article  CAS  Google Scholar 

  78. 78

    Feldman, D.E. & Brecht, M. Map plasticity in somatosensory cortex. Science 310, 810–815 (2005).

    Article  CAS  Google Scholar 

  79. 79

    Shepherd, G.M.G., Stepanyants, A., Bureau, I., Chklovskii, D. & Svoboda, K. Geometric and functional organization of cortical circuits. Nat. Neurosci. 8, 782–790 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. 80

    Vélez-Fort, M. et al. The stimulus selectivity and connectivity of layer six principal cells reveals cortical microcircuits underlying visual processing. Neuron 83, 1431–1443 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. 81

    Watakabe, A. et al. Area-specific substratification of deep layer neurons in the rat cortex. J. Comp. Neurol. 520, 3553–3573 (2012).

    Article  CAS  Google Scholar 

  82. 82

    Bai, W.Z., Ishida, M. & Arimatsu, Y. Chemically defined feedback connections from infragranular layers of sensory association cortices in the rat. Neuroscience 123, 257–267 (2004).

    Article  CAS  Google Scholar 

  83. 83

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

    Article  CAS  Google Scholar 

  84. 84

    Tamamaki, N. & Tomioka, R. Long-range GABAergic connections distributed throughout the neocortex and their possible function. Front. Neurosci. 4, 202 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. 85

    Constantinople, C.M. & Bruno, R.M. Deep cortical layers are activated directly by thalamus. Science 340, 1591–1594 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. 86

    Kita, T. & Kita, H. The subthalamic nucleus is one of multiple innervation sites for long-range corticofugal axons: a single-axon tracing study in the rat. J. Neurosci. 32, 5990–5999 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. 87

    Ueta, Y., Hirai, Y., Otsuka, T. & Kawaguchi, Y. Direction- and distance-dependent interareal connectivity of pyramidal cell subpopulations in the rat frontal cortex. Front. Neural Circuits 7, 164 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  88. 88

    Nelson, A. et al. A circuit for motor cortical modulation of auditory cortical activity. J. Neurosci. 33, 14342–14353 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. 89

    Veinante, P. & Deschenes, M. Single-cell study of motor cortex projections to the barrel field in rats. J. Comp. Neurol. 464, 98–103 (2003).

    Article  Google Scholar 

  90. 90

    Sheets, P.L. et al. Corticospinal-specific HCN expression in mouse motor cortex: Ih-dependent synaptic integration as a candidate microcircuit mechanism involved in motor control. J. Neurophysiol. 106, 2216–2231 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  91. 91

    Suter, B.A., Migliore, M. & Shepherd, G.M.G. Intrinsic electrophysiology of mouse corticospinal neurons: a class-specific triad of spike-related properties. Cereb. Cortex 23, 1965–1977 (2013).

    Article  Google Scholar 

  92. 92

    Dembrow, N. & Johnston, D. Subcircuit-specific neuromodulation in the prefrontal cortex. Front. Neural Circuits 8, 54 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  93. 93

    Miller, M.N., Okaty, B.W. & Nelson, S.B. Region-specific spike-frequency acceleration in layer 5 pyramidal neurons mediated by Kv1 subunits. J. Neurosci. 28, 13716–13726 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. 94

    Tseng, G.F. & Prince, D.A. Heterogeneity of rat corticospinal neurons. J. Comp. Neurol. 335, 92–108 (1993).

    Article  CAS  Google Scholar 

  95. 95

    Phillips, C.G. & Porter, R. Corticospinal Neurones: Their Role in Movement (Academic, London, 1977).

  96. 96

    Christophe, E. et al. Two populations of layer V pyramidal cells of the mouse neocortex: development and sensitivity to anesthetics. J. Neurophysiol. 94, 3357–3367 (2005).

    Article  CAS  Google Scholar 

  97. 97

    de Kock, C.P. & Sakmann, B. High frequency action potential bursts (≥100 Hz) in L2/3 and L5B thick tufted neurons in anaesthetized and awake rat primary somatosensory cortex. J. Physiol. (Lond.) 586, 3353–3364 (2008).

    Article  CAS  Google Scholar 

  98. 98

    Beloozerova, I.N. et al. Activity of different classes of neurons of the motor cortex during postural corrections. J. Neurosci. 23, 7844–7853 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. 99

    Swadlow, H.A. Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties. J. Neurophysiol. 62, 288–308 (1989).

    Article  CAS  Google Scholar 

  100. 100

    da Costa, N.M. & Martin, K.A. Selective targeting of the dendrites of corticothalamic cells by thalamic afferents in area 17 of the cat. J. Neurosci. 29, 13919–13928 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. 101

    Zhang, Z.W. & Deschenes, M. Projections to layer VI of the posteromedial barrel field in the rat: a reappraisal of the role of corticothalamic pathways. Cereb. Cortex 8, 428–436 (1998).

    Article  CAS  Google Scholar 

  102. 102

    Deschênes, M., Veinante, P. & Zhang, Z.W. The organization of corticothalamic projections: reciprocity versus parity. Brain Res. Brain Res. Rev. 28, 286–308 (1998).

    Article  Google Scholar 

  103. 103

    Guillery, R.W. & Sherman, S.M. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33, 163–175 (2002).

    Article  CAS  Google Scholar 

  104. 104

    Zhang, Z.W. & Deschenes, M. Intracortical axonal projections of lamina VI cells of the primary somatosensory cortex in the rat: a single-cell labeling study. J. Neurosci. 17, 6365–6379 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. 105

    Bortone, D.S., Olsen, S.R. & Scanziani, M. Translaminar inhibitory cells recruited by layer 6 corticothalamic neurons suppress visual cortex. Neuron 82, 474–485 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. 106

    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 65, 230–245 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. 107

    Sirota, M.G., Swadlow, H.A. & Beloozerova, I.N. Three channels of corticothalamic communication during locomotion. J. Neurosci. 25, 5915–5925 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. 108

    Markov, N.T. et al. Cortical high-density counterstream architectures. Science 342, 1238406 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. 109

    Oh, S.W. et al. A mesoscale connectome of the mouse brain. Nature 508, 207–214 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. 110

    Zingg, B. et al. Neural networks of the mouse neocortex. Cell 156, 1096–1111 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. 111

    Berezovskii, V.K., Nassi, J.J. & Born, R.T. Segregation of feedforward and feedback projections in mouse visual cortex. J. Comp. Neurol. 519, 3672–3683 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  112. 112

    Mao, T. et al. Long-range neuronal circuits underlying the interaction between sensory and motor cortex. Neuron 72, 111–123 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. 113

    Movshon, J.A. & Newsome, W.T. Visual response properties of striate cortical neurons projecting to area MT in macaque monkeys. J. Neurosci. 16, 7733–7741 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. 114

    DeFelipe, J. et al. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14, 202–216 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. 115

    Rudy, B. et al. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71, 45–61 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  116. 116

    Kepecs, A. & Fishell, G. Interneuron cell types are fit to function. Nature 505, 318–326 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. 117

    Taniguchi, H. Genetic dissection of GABAergic neural circuits in mouse neocortex. Front. Cell. Neurosci. 8, 8 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. 118

    Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53–57 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. 119

    Pi, H.J. et al. Cortical interneurons that specialize in disinhibitory control. Nature 503, 521–524 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. 120

    Lee, S., Kruglikov, I., Huang, Z.J., Fishell, G. & Rudy, B. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat. Neurosci. 16, 1662–1670 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. 121

    Pfeffer, C.K., Xue, M., He, M., Huang, Z.J. & Scanziani, M. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16, 1068–1076 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. 122

    Jiang, X., Wang, G., Lee, A.J., Stornetta, R.L. & Zhu, J.J. The organization of two new cortical interneuronal circuits. Nat. Neurosci. 16, 210–218 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. 123

    Cruikshank, S.J. et al. Thalamic control of layer 1 circuits in prefrontal cortex. J. Neurosci. 32, 17813–17823 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. 124

    Fu, Y. et al. A cortical circuit for gain control by behavioral state. Cell 156, 1139–1152 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. 125

    Zhang, S. et al. Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing. Science 345, 660–665 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. 126

    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. 33, 17373–17384 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. 127

    Xu, H., Jeong, H.Y., Tremblay, R. & Rudy, B. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 77, 155–167 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. 128

    Gentet, L.J. et al. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 607–612 (2012).

    Article  CAS  Google Scholar 

  129. 129

    Xu, N.L. et al. Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 492, 247–251 (2012).

    Article  CAS  Google Scholar 

  130. 130

    Saleem, A.B., Ayaz, A., Jeffery, K.J., Harris, K.D. & Carandini, M. Integration of visual motion and locomotion in mouse visual cortex. Nat. Neurosci. 16, 1864–1869 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. 131

    Bennett, C., Arroyo, S. & Hestrin, S. Subthreshold mechanisms underlying state-dependent modulation of visual responses. Neuron 80, 350–357 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. 132

    Polack, P.O., Friedman, J. & Golshani, P. Cellular mechanisms of brain state-dependent gain modulation in visual cortex. Nat. Neurosci. 16, 1331–1339 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. 133

    Niell, C.M. & Stryker, M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65, 472–479 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. 134

    Schneider, D.M., Nelson, A. & Mooney, R. A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 513, 189–194 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. 135

    Curtis, J.C. & Kleinfeld, D. Phase-to-rate transformations encode touch in cortical neurons of a scanning sensorimotor system. Nat. Neurosci. 12, 492–501 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. 136

    Geschwind, D.H. & Rakic, P. Cortical evolution: judge the brain by its cover. Neuron 80, 633–647 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. 137

    Deck, M. et al. Pathfinding of corticothalamic axons relies on a rendezvous with thalamic projections. Neuron 77, 472–484 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. 138

    Harwell, C.C. et al. Sonic hedgehog expression in corticofugal projection neurons directs cortical microcircuit formation. Neuron 73, 1116–1126 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. 139

    De la Rossa, A. et al. In vivo reprogramming of circuit connectivity in postmitotic neocortical neurons. Nat. Neurosci. 16, 193–200 (2013).

    Article  CAS  Google Scholar 

  140. 140

    Jensen, K.F. & Killackey, H.P. Subcortical projections from ectopic neocortical neurons. Proc. Natl. Acad. Sci. USA 81, 964–968 (1984).

    Article  CAS  Google Scholar 

  141. 141

    Imai, H., Yamamoto, T., Katsuyama, Y., Kikkawa, S. & Terashima, T. Subcortically and callosally projecting neurons are distinct neuronal pools in the motor cortex of the reeler mouse. Kobe J. Med. Sci. 58, E86–E95 (2012).

    PubMed  Google Scholar 

  142. 142

    O'Leary, D.D., Chou, S.J. & Sahara, S. Area patterning of the mammalian cortex. Neuron 56, 252–269 (2007).

    Article  CAS  Google Scholar 

  143. 143

    Chou, S.J. et al. Geniculocortical input drives genetic distinctions between primary and higher-order visual areas. Science 340, 1239–1242 (2013).

    Article  CAS  Google Scholar 

  144. 144

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

    Article  PubMed  PubMed Central  Google Scholar 

  145. 145

    Callaway, E.M. & Borrell, V. Developmental sculpting of dendritic morphology of layer 4 neurons in visual cortex: influence of retinal input. J. Neurosci. 31, 7456–7470 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. 146

    Wong, P. & Kaas, J.H. An architectonic study of the neocortex of the short-tailed opossum (Monodelphis domestica). Brain Behav. Evol. 73, 206–228 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  147. 147

    Dugas-Ford, J., Rowell, J.J. & Ragsdale, C.W. Cell-type homologies and the origins of the neocortex. Proc. Natl. Acad. Sci. USA 109, 16974–16979 (2012).

    Article  Google Scholar 

  148. 148

    Catania, K.C. Evolution of brains and behavior for optimal foraging: a tale of two predators. Proc. Natl. Acad. Sci. USA 109 (suppl. 1), 10701–10708 (2012).

    Article  Google Scholar 

  149. 149

    Hutsler, J.J., Lee, D.G. & Porter, K.K. Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species. Brain Res. 1052, 71–81 (2005).

    Article  CAS  Google Scholar 

  150. 150

    Taniguchi, H. et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995–1013 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank K. Svoboda, N. Steinmetz, N. Yamawaki and M. Carandini for comments. K.D.H. is supported by grants from the Wellcome Trust (095668), Engineering and Physical Sciences Research Council (I005102, K015141) and Simons Foundation. G.M.G.S. is supported by grants from the US National Institutes of Health (NS061963, NS087479, DC013272, EB017695) and the Whitehall Foundation.

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Correspondence to Kenneth D Harris or Gordon M G Shepherd.

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Harris, K., Shepherd, G. The neocortical circuit: themes and variations. Nat Neurosci 18, 170–181 (2015). https://doi.org/10.1038/nn.3917

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