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.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
A frontal transcallosal inhibition loop mediates interhemispheric balance in visuospatial processing
Nature Communications Open Access 25 August 2023
-
Mechanisms underlying pathological cortical bursts during metabolic depletion
Nature Communications Open Access 08 August 2023
-
Cell-type-specific plasticity of inhibitory interneurons in the rehabilitation of auditory cortex after peripheral damage
Nature Communications Open Access 13 July 2023
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout






References
Douglas, R.J., Martin, K.A. & Whitteridge, D. A canonical microcircuit for neocortex. Neural Comput. 1, 480–488 (1989).
Douglas, R.J. & Martin, K.A. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419–451 (2004).
Thomson, A.M. & Lamy, C. Functional maps of neocortical local circuitry. Front. Neurosci. 1, 19–42 (2007).
Harris, K.D. & Mrsic-Flogel, T.D. Cortical connectivity and sensory coding. Nature 503, 51–58 (2013).
Braitenberg, V.B. & Schuz, A. Cortex: Statistics and Geometry of Neuronal Connectivity (Springer, Berlin, 1998).
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).
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).
Feldmeyer, D. Excitatory neuronal connectivity in the barrel cortex. Front. Neuroanat. 6, 24 (2012).
Ko, H. et al. Functional specificity of local synaptic connections in neocortical networks. Nature 473, 87–91 (2011).
Shepherd, G.M.G. Corticostriatal connectivity and its role in disease. Nat. Rev. Neurosci. 14, 278–291 (2013).
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).
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).
Huang, Z.J. Toward a genetic dissection of cortical circuits in the mouse. Neuron 83, 1284–1302 (2014).
von Economo, C. The Cytoarchitectonics of the Human Cerebral Cortex (Oxford Univ. Press, London, 1929).
Morishima, M. & Kawaguchi, Y. Recurrent connection patterns of corticostriatal pyramidal cells in frontal cortex. J. Neurosci. 26, 4394–4405 (2006).
Petreanu, L., Mao, T., Sternson, S.M. & Svoboda, K. The subcellular organization of neocortical excitatory connections. Nature 457, 1142–1145 (2009).
Brown, S.P. & Hestrin, S. Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457, 1133–1136 (2009).
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).
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).
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).
Evarts, E.V., Shinoda, Y. & Wise, S.P. Neurophysiological Approaches to Higher Brain Functions (Wiley, New York, 1984).
Jones, E.G. The thalamic matrix and thalamocortical synchrony. Trends Neurosci. 24, 595–601 (2001).
Clascá, F., Rubio-Garrido, P. & Jabaudon, D. Unveiling the diversity of thalamocortical neuron subtypes. Eur. J. Neurosci. 35, 1524–1532 (2012).
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).
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).
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).
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).
Nassi, J.J. & Callaway, E.M. Parallel processing strategies of the primate visual system. Nat. Rev. Neurosci. 10, 360–372 (2009).
Herkenham, M. Laminar organization of thalamic projections to the rat neocortex. Science 207, 532–535 (1980).
Cruz-Martín, A. et al. A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex. Nature 507, 358–361 (2014).
Kaneko, T. Local connections of excitatory neurons in motor-associated cortical areas of the rat. Front. Neural Circuits 7, 75 (2013).
Hooks, B.M. et al. Laminar organization of long-range excitatory input to mouse motor cortex. J. Neurosci. 33, 748–760 (2013).
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).
Pouchelon, G. et al. Modality-specific thalamocortical inputs instruct the identity of postsynaptic L4 neurons. Nature 511, 471–474 (2014).
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).
Thomson, A.M. Neocortical layer 6, a review. Front. Neuroanat. 4, 13 (2010).
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).
Hooks, B.M. et al. Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas. PLoS Biol. 9, e1000572 (2011).
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).
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).
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).
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).
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).
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).
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).
Zhou, M. et al. Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. Nat. Neurosci. 17, 841–850 (2014).
Hansen, B.J., Chelaru, M.I. & Dragoi, V. Correlated variability in laminar cortical circuits. Neuron 76, 590–602 (2012).
Smith, M.A., Jia, X., Zandvakili, A. & Kohn, A. Laminar dependence of neuronal correlations in visual cortex. J. Neurophysiol. 109, 940–947 (2013).
Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).
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).
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).
Swadlow, H.A. Thalamocortical control of feed-forward inhibition in awake somatosensory 'barrel' cortex. Phil. Trans. R. Soc. Lond. B 357, 1717–1727 (2002).
Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442–446 (2003).
Wilent, W.B. & Contreras, D. Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat. Neurosci. 8, 1364–1370 (2005).
Shepherd, G.M.G. Intracortical cartography in an agranular area. Front. Neurosci. 3, 337–343 (2009).
Alfano, C. & Studer, M. Neocortical arealization: evolution, mechanisms, and open questions. Dev. Neurobiol. 73, 411–447 (2013).
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).
García-Cabezas, M.A. & Barbas, H. Area 4 has layer IV in adult primates. Eur. J. Neurosci. 39, 1824–1834 (2014).
Coogan, T.A. & Burkhalter, A. Hierarchical organization of areas in rat visual cortex. J. Neurosci. 13, 3749–3772 (1993).
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).
Markov, N.T. & Kennedy, H. The importance of being hierarchical. Curr. Opin. Neurobiol. 23, 187–194 (2013).
Petreanu, L., Huber, D., Sobczyk, A. & Svoboda, K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10, 663–668 (2007).
Adesnik, H. & Scanziani, M. Lateral competition for cortical space by layer-specific horizontal circuits. Nature 464, 1155–1160 (2010).
Sato, T.R. & Svoboda, K. The functional properties of barrel cortex neurons projecting to the primary motor cortex. J. Neurosci. 30, 4256–4260 (2010).
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).
Yamashita, T. et al. Membrane potential dynamics of neocortical projection neurons driving target-specific signals. Neuron 80, 1477–1490 (2013).
Bureau, I., Shepherd, G.M.G. & Svoboda, K. Precise development of functional and anatomical columns in the neocortex. Neuron 42, 789–801 (2004).
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).
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).
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).
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).
Sakata, S. & Harris, K.D. Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 64, 404–418 (2009).
Niell, C.M. & Stryker, M.P. Highly selective receptive fields in mouse visual cortex. J. Neurosci. 28, 7520–7536 (2008).
Hromádka, T., Deweese, M.R. & Zador, A.M. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol. 6, e16 (2008).
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).
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).
Diamond, M.E., Huang, W. & Ebner, F.F. Laminar comparison of somatosensory cortical plasticity. Science 265, 1885–1888 (1994).
Feldman, D.E. & Brecht, M. Map plasticity in somatosensory cortex. Science 310, 810–815 (2005).
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).
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).
Watakabe, A. et al. Area-specific substratification of deep layer neurons in the rat cortex. J. Comp. Neurol. 520, 3553–3573 (2012).
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).
Kanold, P.O. & Luhmann, H.J. The subplate and early cortical circuits. Annu. Rev. Neurosci. 33, 23–48 (2010).
Tamamaki, N. & Tomioka, R. Long-range GABAergic connections distributed throughout the neocortex and their possible function. Front. Neurosci. 4, 202 (2010).
Constantinople, C.M. & Bruno, R.M. Deep cortical layers are activated directly by thalamus. Science 340, 1591–1594 (2013).
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).
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).
Nelson, A. et al. A circuit for motor cortical modulation of auditory cortical activity. J. Neurosci. 33, 14342–14353 (2013).
Veinante, P. & Deschenes, M. Single-cell study of motor cortex projections to the barrel field in rats. J. Comp. Neurol. 464, 98–103 (2003).
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).
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).
Dembrow, N. & Johnston, D. Subcircuit-specific neuromodulation in the prefrontal cortex. Front. Neural Circuits 8, 54 (2014).
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).
Tseng, G.F. & Prince, D.A. Heterogeneity of rat corticospinal neurons. J. Comp. Neurol. 335, 92–108 (1993).
Phillips, C.G. & Porter, R. Corticospinal Neurones: Their Role in Movement (Academic, London, 1977).
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).
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).
Beloozerova, I.N. et al. Activity of different classes of neurons of the motor cortex during postural corrections. J. Neurosci. 23, 7844–7853 (2003).
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).
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).
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).
Deschênes, M., Veinante, P. & Zhang, Z.W. The organization of corticothalamic projections: reciprocity versus parity. Brain Res. Brain Res. Rev. 28, 286–308 (1998).
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).
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).
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).
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).
Sirota, M.G., Swadlow, H.A. & Beloozerova, I.N. Three channels of corticothalamic communication during locomotion. J. Neurosci. 25, 5915–5925 (2005).
Markov, N.T. et al. Cortical high-density counterstream architectures. Science 342, 1238406 (2013).
Oh, S.W. et al. A mesoscale connectome of the mouse brain. Nature 508, 207–214 (2014).
Zingg, B. et al. Neural networks of the mouse neocortex. Cell 156, 1096–1111 (2014).
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).
Mao, T. et al. Long-range neuronal circuits underlying the interaction between sensory and motor cortex. Neuron 72, 111–123 (2011).
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).
DeFelipe, J. et al. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14, 202–216 (2013).
Rudy, B. et al. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71, 45–61 (2011).
Kepecs, A. & Fishell, G. Interneuron cell types are fit to function. Nature 505, 318–326 (2014).
Taniguchi, H. Genetic dissection of GABAergic neural circuits in mouse neocortex. Front. Cell. Neurosci. 8, 8 (2014).
Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53–57 (2008).
Pi, H.J. et al. Cortical interneurons that specialize in disinhibitory control. Nature 503, 521–524 (2013).
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).
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).
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).
Cruikshank, S.J. et al. Thalamic control of layer 1 circuits in prefrontal cortex. J. Neurosci. 32, 17813–17823 (2012).
Fu, Y. et al. A cortical circuit for gain control by behavioral state. Cell 156, 1139–1152 (2014).
Zhang, S. et al. Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing. Science 345, 660–665 (2014).
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).
Xu, H., Jeong, H.Y., Tremblay, R. & Rudy, B. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 77, 155–167 (2013).
Gentet, L.J. et al. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 607–612 (2012).
Xu, N.L. et al. Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 492, 247–251 (2012).
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).
Bennett, C., Arroyo, S. & Hestrin, S. Subthreshold mechanisms underlying state-dependent modulation of visual responses. Neuron 80, 350–357 (2013).
Polack, P.O., Friedman, J. & Golshani, P. Cellular mechanisms of brain state-dependent gain modulation in visual cortex. Nat. Neurosci. 16, 1331–1339 (2013).
Niell, C.M. & Stryker, M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65, 472–479 (2010).
Schneider, D.M., Nelson, A. & Mooney, R. A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 513, 189–194 (2014).
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).
Geschwind, D.H. & Rakic, P. Cortical evolution: judge the brain by its cover. Neuron 80, 633–647 (2013).
Deck, M. et al. Pathfinding of corticothalamic axons relies on a rendezvous with thalamic projections. Neuron 77, 472–484 (2013).
Harwell, C.C. et al. Sonic hedgehog expression in corticofugal projection neurons directs cortical microcircuit formation. Neuron 73, 1116–1126 (2012).
De la Rossa, A. et al. In vivo reprogramming of circuit connectivity in postmitotic neocortical neurons. Nat. Neurosci. 16, 193–200 (2013).
Jensen, K.F. & Killackey, H.P. Subcortical projections from ectopic neocortical neurons. Proc. Natl. Acad. Sci. USA 81, 964–968 (1984).
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).
O'Leary, D.D., Chou, S.J. & Sahara, S. Area patterning of the mammalian cortex. Neuron 56, 252–269 (2007).
Chou, S.J. et al. Geniculocortical input drives genetic distinctions between primary and higher-order visual areas. Science 340, 1239–1242 (2013).
Erzurumlu, R.S. & Gaspar, P. Development and critical period plasticity of the barrel cortex. Eur. J. Neurosci. 35, 1540–1553 (2012).
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).
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).
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).
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).
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).
Taniguchi, H. et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995–1013 (2011).
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.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Rights and permissions
About this article
Cite this article
Harris, K., Shepherd, G. The neocortical circuit: themes and variations. Nat Neurosci 18, 170–181 (2015). https://doi.org/10.1038/nn.3917
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn.3917
This article is cited by
-
Cell-type-specific plasticity of inhibitory interneurons in the rehabilitation of auditory cortex after peripheral damage
Nature Communications (2023)
-
Mechanisms underlying pathological cortical bursts during metabolic depletion
Nature Communications (2023)
-
Cortical glutamatergic projection neuron types contribute to distinct functional subnetworks
Nature Neuroscience (2023)
-
Interacting spiral wave patterns underlie complex brain dynamics and are related to cognitive processing
Nature Human Behaviour (2023)
-
Primary somatosensory cortex bidirectionally modulates sensory gain and nociceptive behavior in a layer-specific manner
Nature Communications (2023)