Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Cortical connectivity and sensory coding

Subjects

Abstract

The sensory cortex contains a wide array of neuronal types, which are connected together into complex but partially stereotyped circuits. Sensory stimuli trigger cascades of electrical activity through these circuits, causing specific features of sensory scenes to be encoded in the firing patterns of cortical populations. Recent research is beginning to reveal how the connectivity of individual neurons relates to the sensory features they encode, how differences in the connectivity patterns of different cortical cell classes enable them to encode information using different strategies, and how feedback connections from higher-order cortex allow sensory information to be integrated with behavioural context.

This is a preview of subscription content, access via your institution

Access options

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

Figure 1: Proposed fine structure of neocortical connections.
Figure 2: Coding strategies of different cortical layers.
Figure 3: Proposed relationship between feature mapping and coding in rodent visual cortex, cat visual cortex and rodent auditory cortex.

Similar content being viewed by others

References

  1. Quian Quiroga, R. & Panzeri, S. Principles of Neural Coding. (CRC Press, 2013)

    Book  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. Gong, S. et al. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425, 917–925 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  5. Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nature Neurosci. 13, 133–140 (2010)

    Article  CAS  PubMed  Google Scholar 

  6. Taniguchi, H. et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995–1013 (2011); erratum. 72, 1091 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Buzsáki, G. Large-scale recording of neuronal ensembles. Nature Neurosci. 7, 446–451 (2004)

    Article  CAS  PubMed  Google Scholar 

  8. Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  10. Bock, D. D. et al. Network anatomy and in vivo physiology of visual cortical neurons. Nature 471, 177–182 (2011)Together with ref. 26 , this paper shows that synaptic connections from principal cells to interneurons are nonspecific with respect to sensory tuning.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  11. Briggman, K. L., Helmstaedter, M. & Denk, W. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183–188 (2011)

    Article  ADS  CAS  PubMed  Google Scholar 

  12. Fenno, L., Yizhar, O. & Deisseroth, K. The development and application of optogenetics. Annu. Rev. Neurosci. 34, 389–412 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Song, S., Sjostrom, P. J., Reigl, M., Nelson, S. & Chklovskii, D. B. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 3, e68 (2005)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Perin, R., Berger, T. K. & Markram, H. A synaptic organizing principle for cortical neuronal groups. Proc. Natl Acad. Sci. USA 108, 5419–5424 (2011)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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  Google Scholar 

  16. Yoshimura, Y., Dantzker, J. L. & Callaway, E. M. Excitatory cortical neurons form fine-scale functional networks. Nature 433, 868–873 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Otsuka, T. & Kawaguchi, Y. Cell diversity and connection specificity between callosal projection neurons in the frontal cortex. J. Neurosci. 31, 3862–3870 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Packer, A. M. & Yuste, R. Dense, unspecific connectivity of neocortical parvalbumin-positive interneurons: a canonical microcircuit for inhibition? J. Neurosci. 31, 13260–13271 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Fino, E. & Yuste, R. Dense inhibitory connectivity in neocortex. Neuron 69, 1188–1203 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ko, H. et al. Functional specificity of local synaptic connections in neocortical networks. Nature 473, 87–91 (2011)This paper shows that receptive field similarity and neuronal correlations are higher for connected than unconnected pairs of principal cells in superficial mouse visual cortex.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sun, Y. J., Kim, Y. J., Ibrahim, L. A., Tao, H. W. & Zhang, L. I. Synaptic mechanisms underlying functional dichotomy between intrinsic-bursting and regular-spiking neurons in auditory cortical layer 5. J. Neurosci. 33, 5326–5339 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lien, A. D. & Scanziani, M. Tuned thalamic excitation is amplified by visual cortical circuits. Nature Neurosci. 16, 1315–1323 (2013)

    Article  CAS  PubMed  Google Scholar 

  23. Li, L. Y., Li, Y. T., Zhou, M., Tao, H. W. & Zhang, L. I. Intracortical multiplication of thalamocortical signals in mouse auditory cortex. Nature Neurosci. 16, 1179–1181 (2013)

    Article  CAS  PubMed  Google Scholar 

  24. Li, Y. T., Ibrahim, L. A., Liu, B. H., Zhang, L. I. & Tao, H. W. Linear transformation of thalamocortical input by intracortical excitation. Nature Neurosci. 16, 1324–1330 (2013)References 21, 22, 23, 24 show that the thalamic and intracortical excitatory inputs a principal cell receives are similarly tuned.

    Article  CAS  PubMed  Google Scholar 

  25. Gilbert, C. D. & Wiesel, T. N. Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J. Neurosci. 9, 2432–2442 (1989)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hofer, S. B. et al. Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nature Neurosci. 14, 1045–1052 (2011)

    Article  CAS  PubMed  Google Scholar 

  27. Douglas, R. J., Koch, C., Mahowald, M., Martin, K. A. & Suarez, H. H. Recurrent excitation in neocortical circuits. Science 269, 981–985 (1995)

    Article  ADS  CAS  PubMed  Google Scholar 

  28. Gao, P., Sultan, K. T., Zhang, X. J. & Shi, S. H. Lineage-dependent circuit assembly in the neocortex. Development 140, 2645–2655 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Yu, Y. C. et al. Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly. Nature 486, 113–117 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ko, H. et al. The emergence of functional microcircuits in visual cortex. Nature 496, 96–100 (2013)This paper shows that the relationship between sensory tuning and synaptic connectivity is weak at eye opening but grows stronger after visual experience.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hebb, D. O. The Organization of Behavior. (Wiley, 1949)

    Google Scholar 

  32. Feldman, D. E. Synaptic mechanisms for plasticity in neocortex. Annu. Rev. Neurosci. 32, 33–55 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Yger, P. & Harris, K. D. The Convallis rule for unsupervised learning in cortical networks. PLoS Comput. Biol (in the press)

  34. Harris, K. D. Stability of the fittest: organizing learning through retroaxonal signals. Trends Neurosci. 31, 130–136 (2008)

    Article  CAS  PubMed  Google Scholar 

  35. Clopath, C., Busing, L., Vasilaki, E. & Gerstner, W. Connectivity reflects coding: a model of voltage-based STDP with homeostasis. Nature Neurosci. 13, 344–352 (2010)

    Article  CAS  PubMed  Google Scholar 

  36. Willmore, B. & Tolhurst, D. J. Characterizing the sparseness of neural codes. Network 12, 255–270 (2001)

    Article  CAS  PubMed  Google Scholar 

  37. Olshausen, B. A. & Field, D. J. Sparse coding of sensory inputs. Curr. Opin. Neurobiol. 14, 481–487 (2004)

    Article  CAS  PubMed  Google Scholar 

  38. Gardner-Medwin, A. R. The recall of events through the learning of associations between their parts. Proc. R. Soc. Lond. B Biol. Sci. 194, 375–402 (1976)

    Article  ADS  CAS  PubMed  Google Scholar 

  39. 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  Google Scholar 

  40. 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 

  41. 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 

  42. Niell, C. M. & Stryker, M. P. Highly selective receptive fields in mouse visual cortex. J. Neurosci. 28, 7520–7536 (2008)References 39, 40, 41, 42 show that in rodent auditory, somatosensory and visual cortex, superficial principal cells fire sparsely and selectively, whereas deep SPNs and putative interneurons of all layers fire densely and with broad sensory tuning.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Meyer, H. S. et al. Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A. Proc. Natl Acad. Sci. USA 108, 16807–16812 (2011)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  44. Haider, B., Hausser, M. & Carandini, M. Inhibition dominates sensory responses in the awake cortex. Nature 493, 97–100 (2013)

    Article  ADS  CAS  PubMed  Google Scholar 

  45. Mateo, C. et al. In vivo optogenetic stimulation of neocortical excitatory neurons drives brain-state-dependent inhibition. Curr. Biol. 21, 1593–1602 (2011)

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  47. Adesnik, H., Bruns, W., Taniguchi, H., Huang, Z. J. & Scanziani, M. A neural circuit for spatial summation in visual cortex. Nature 490, 226–231 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  48. Beltramo, R. et al. Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex. Nature Neurosci. 16, 227–234 (2013)References 45, 46, 47, 48 show that optogenetic stimulation of superficial layer principal cells causes predominant inhibition in neighbouring neurons, whereas stimulation of deep layer principal cells causes predominant excitation.

    Article  CAS  PubMed  Google Scholar 

  49. Bathellier, B., Ushakova, L. & Rumpel, S. Discrete neocortical dynamics predict behavioral categorization of sounds. Neuron 76, 435–449 (2012)

    Article  CAS  PubMed  Google Scholar 

  50. 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  PubMed  Google Scholar 

  51. Hefti, B. J. & Smith, P. H. Anatomy, physiology, and synaptic responses of rat layer V auditory cortical cells and effects of intracellular GABA(A) blockade. J. Neurophysiol. 83, 2626–2638 (2000)

    Article  CAS  PubMed  Google Scholar 

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

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  53. Kampa, B. M., Letzkus, J. J. & Stuart, G. J. Cortical feed-forward networks for binding different streams of sensory information. Nature Neurosci. 9, 1472–1473 (2006)

    Article  CAS  PubMed  Google Scholar 

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

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  55. Schubert, D., Kotter, R. & Staiger, J. F. Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits. Brain Struct. Funct. 212, 107–119 (2007)

    Article  PubMed  Google Scholar 

  56. Stroh, A. et al. Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo. Neuron 77, 1136–1150 (2013)

    Article  CAS  PubMed  Google Scholar 

  57. Kerlin, A. M., Andermann, M. L., Berezovskii, V. K. & Reid, R. C. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 67, 858–871 (2010)This paper shows that in mouse superficial visual cortex, the sensory tuning of parvalbumin-, somatostatin- and vasoactive-intestinal-peptide-expressing interneurons approximates the average tuning of neighbouring principal cells.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Sohya, K., Kameyama, K., Yanagawa, Y., Obata, K. & Tsumoto, T. GABAergic neurons are less selective to stimulus orientation than excitatory neurons in layer II/III of visual cortex, as revealed by in vivo functional Ca2+ imaging in transgenic mice. J. Neurosci. 27, 2145–2149 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Liu, B. H. et al. Visual receptive field structure of cortical inhibitory neurons revealed by two-photon imaging guided recording. J. Neurosci. 29, 10520–10532 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Runyan, C. A. & Sur, M. Response selectivity is correlated to dendritic structure in parvalbumin-expressing inhibitory neurons in visual cortex. J. Neurosci. 33, 11724–11733 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Ohki, K., Chung, S., Ch'ng, Y. H., Kara, P. & Reid, R. C. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433, 597–603 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  62. Van Hooser, S. D., Heimel, J. A., Chung, S. & Nelson, S. B. Lack of patchy horizontal connectivity in primary visual cortex of a mammal without orientation maps. J. Neurosci. 26, 7680–7692 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Jia, H., Rochefort, N. L., Chen, X. & Konnerth, A. Dendritic organization of sensory input to cortical neurons in vivo. Nature 464, 1307–1312 (2010)

    Article  ADS  CAS  PubMed  Google Scholar 

  64. Mariño, J. et al. Invariant computations in local cortical networks with balanced excitation and inhibition. Nature Neurosci. 8, 194–201 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  65. Wu, G. K., Arbuckle, R., Liu, B. H., Tao, H. W. & Zhang, L. I. Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron 58, 132–143 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Tan, A. Y., Brown, B. D., Scholl, B., Mohanty, D. & Priebe, N. J. Orientation selectivity of synaptic input to neurons in mouse and cat primary visual cortex. J. Neurosci. 31, 12339–12350 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Carandini, M. & Ferster, D. Membrane potential and firing rate in cat primary visual cortex. J. Neurosci. 20, 470–484 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Cardin, J. A., Palmer, L. A. & Contreras, D. Stimulus feature selectivity in excitatory and inhibitory neurons in primary visual cortex. J. Neurosci. 27, 10333–10344 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Liu, B. H. et al. Broad inhibition sharpens orientation selectivity by expanding input dynamic range in mouse simple cells. Neuron 71, 542–554 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Luczak, A., Bartho, P. & Harris, K. D. Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron 62, 413–425 (2009)This paper shows that the firing patterns a cortical population can produce are subject to preserved constraints on the timing and combinations of neurons that may be active together.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Smith, M. A. & Kohn, A. Spatial and temporal scales of neuronal correlation in primary visual cortex. J. Neurosci. 28, 12591–12603 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Schneidman, E., Berry, M. J., II, Segev, R. & Bialek, W. Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440, 1007–1012 (2006)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  73. Barlow, H. Redundancy reduction revisited. Network 12, 241–253 (2001)

    Article  CAS  PubMed  Google Scholar 

  74. Chechik, G. et al. Reduction of information redundancy in the ascending auditory pathway. Neuron 51, 359–368 (2006)

    Article  CAS  PubMed  Google Scholar 

  75. Shuler, M. G. & Bear, M. F. Reward timing in the primary visual cortex. Science 311, 1606–1609 (2006)

    Article  ADS  CAS  PubMed  Google Scholar 

  76. Keller, G. B., Bonhoeffer, T. & Hubener, M. Sensorimotor mismatch signals in primary visual cortex of the behaving mouse. Neuron 74, 809–815 (2012)

    Article  CAS  PubMed  Google Scholar 

  77. Jaramillo, S. & Zador, A. M. The auditory cortex mediates the perceptual effects of acoustic temporal expectation. Nature Neurosci. 14, 246–251 (2011)

    Article  CAS  PubMed  Google Scholar 

  78. Reynolds, J. H. & Heeger, D. J. The normalization model of attention. Neuron 61, 168–185 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Saleem, A. B., Ayaz, A., Jeffery, K., Harris, K. D. & Carandini, M. Integration of visual motion and locomotion in mouse visual cortex Nature Neurosci. (in the press)

  80. Poulet, J. F. & Petersen, C. C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454, 881–885 (2008)

    Article  ADS  CAS  PubMed  Google Scholar 

  81. 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 

  82. Petreanu, L. et al. Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 489, 299–303 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  83. Larkum, M. E., Zhu, J. J. & Sakmann, B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398, 338–341 (1999)

    Article  ADS  CAS  PubMed  Google Scholar 

  84. Larkum, M. E., Senn, W. & Luscher, H. R. Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb. Cortex 14, 1059–1070 (2004)

    Article  PubMed  Google Scholar 

  85. Cohen, M. R. & Maunsell, J. H. Using neuronal populations to study the mechanisms underlying spatial and feature attention. Neuron 70, 1192–1204 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Moore, T. & Armstrong, K. M. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421, 370–373 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  87. Moore, T. & Fallah, M. Control of eye movements and spatial attention. Proc. Natl Acad. Sci. USA 98, 1273–1276 (2001)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  89. Lee, S., Kruglikov, I., Huang, Z. J., Fishell, G. & Rudy, B. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nature Neurosci (in the press)

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

    Article  CAS  PubMed  Google Scholar 

  91. Wickersham, I. R., Finke, S., Conzelmann, K. K. & Callaway, E. M. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nature Methods 4, 47–49 (2007)

    Article  CAS  PubMed  Google Scholar 

  92. Kim, J. et al. mGRASP enables mapping mammalian synaptic connectivity with light microscopy. Nature Methods 9, 96–102 (2012)

    Article  ADS  CAS  Google Scholar 

  93. Chung, K. et al. Structural and molecular interrogation of intact biological systems. Nature 497, 332–337 (2013)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  94. Huber, D. et al. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484, 473–478 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  95. 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 

  96. Brecht, M. & Sakmann, B. Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex. J. Physiol. (Lond.) 543, 49–70 (2002)

    Article  CAS  Google Scholar 

  97. 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 

  98. Narboux-Nême, N. et al. Neurotransmitter release at the thalamocortical synapse instructs barrel formation but not axon patterning in the somatosensory cortex. J. Neurosci. 32, 6183–6196 (2012)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Jabaudon, D., Shnider, S. J., Tischfield, D. J., Galazo, M. J. & Macklis, J. D. RORbeta induces barrel-like neuronal clusters in the developing neocortex. Cereb. Cortex 22, 996–1006 (2012)

    Article  PubMed  Google Scholar 

  100. Molyneaux, B. J. et al. Novel subtype-specific genes identify distinct subpopulations of callosal projection neurons. J. Neurosci. 29, 12343–12354 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. 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  ADS  CAS  PubMed  Google Scholar 

  102. Srinivasan, K. et al. A network of genetic repression and derepression specifies projection fates in the developing neocortex. Proc. Natl Acad. Sci. USA 109, 19071–19078 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  103. Groh, A. et al. Cell-type specific properties of pyramidal neurons in neocortex underlying a layout that is modifiable depending on the cortical area. Cereb. Cortex 20, 826–836 (2010)

    Article  PubMed  Google Scholar 

  104. Maruoka, H., Kubota, K., Kurokawa, R., Tsuruno, S. & Hosoya, T. Periodic organization of a major subtype of pyramidal neurons in neocortical layer V. J. Neurosci. 31, 18522–18542 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. 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  PubMed  Google Scholar 

  106. 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 

  107. Matyas, F. et al. Motor control by sensory cortex. Science 330, 1240–1243 (2010)

    Article  ADS  CAS  PubMed  Google Scholar 

  108. Sherman, S. M. Thalamocortical interactions. Curr. Opin. Neurobiol. 22, 575–579 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Reiner, A., Hart, N. M., Lei, W. & Deng, Y. Corticostriatal projection neurons - dichotomous types and dichotomous functions. Front. Neuroanat. 4, 142 (2010)

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  112. Lee, C. C. & Sherman, S. M. Glutamatergic inhibition in sensory neocortex. Cereb. Cortex 19, 2281–2289 (2009)

    Article  PubMed  PubMed Central  Google Scholar 

  113. 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  ADS  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  115. 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. Nature Neurosci. 16, 1068–1076 (2013)

    Article  CAS  PubMed  Google Scholar 

  116. Lewis, D. A., Hashimoto, T. & Volk, D. W. Cortical inhibitory neurons and schizophrenia. Nature Rev. Neurosci. 6, 312–324 (2005)

    Article  CAS  Google Scholar 

  117. 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 

  118. Murayama, M. et al. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457, 1137–1141 (2009)

    Article  ADS  CAS  PubMed  Google Scholar 

  119. Kapfer, C., Glickfeld, L. L., Atallah, B. V. & Scanziani, M. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nature Neurosci. 10, 743–753 (2007)

    Article  CAS  PubMed  Google Scholar 

  120. Silberberg, G. & Markram, H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53, 735–746 (2007)

    Article  CAS  PubMed  Google Scholar 

  121. Sylwestrak, E. L. & Ghosh, A. Elfn1 regulates target-specific release probability at CA1-interneuron synapses. Science 338, 536–540 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  122. Rudy, B., Fishell, G., Lee, S. & Hjerling-Leffler, J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71, 45–61 (2011)

    Article  PubMed  PubMed Central  Google Scholar 

  123. Oláh, S. et al. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461, 1278–1281 (2009)

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  124. Letzkus, J. J. et al. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480, 331–335 (2011)

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank B. Rudy, G. Buzsaki, M. Hausser, B. Haider, S. Hofer, R. Bruno and M. Carandini for comments on the manuscript. K.D.H. is supported by the Wellcome Trust, Engineering and Physical Sciences Research Council and US National Institutes of Health. T.M.-F. is supported by the Wellcome Trust and European Research Council.

Author information

Authors and Affiliations

Authors

Contributions

K.D.H. and T.M.-F. wrote the manuscript.

Corresponding authors

Correspondence to Kenneth D. Harris or Thomas D. Mrsic-Flogel.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harris, K., Mrsic-Flogel, T. Cortical connectivity and sensory coding. Nature 503, 51–58 (2013). https://doi.org/10.1038/nature12654

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature12654

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing