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.

Receptive field structure varies with layer in the primary visual cortex

Abstract

Here we ask whether visual response pattern varies with position in the cortical microcircuit by comparing the structure of receptive fields recorded from the different layers of the cat's primary visual cortex. We used whole-cell recording in vivo to show the spatial distribution of visually evoked excitatory and inhibitory inputs and to stain individual neurons. We quantified the distribution of 'On' and 'Off' responses and the presence of spatially opponent excitation and inhibition within the receptive field. The thalamorecipient layers (4 and upper 6) were dominated by simple cells, as defined by two criteria: they had separated On and Off subregions, and they had push-pull responses (in a given subregion, stimuli of the opposite contrast evoked responses of the opposite sign). Other types of response profile correlated with laminar location as well. Thus, connections unique to each visual cortical layer are likely to serve distinct functions.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Receptive fields with a push-pull arrangement of synaptic inputs.
Figure 2: Receptive fields with push-push or push-null configurations.
Figure 3: The spatial arrangement of On and Off subregions in cortical receptive fields.
Figure 4: Excitation and inhibition within single subregions of the receptive field.
Figure 5: Correlation between receptive field structure and cortical layer.
Figure 7: Laminar distribution of receptive fields with push-pull.
Figure 6: Comparison of subregion overlap and push-pull.
Figure 8: Morphology and receptive field structure.

References

  1. Callaway, E.M. Local circuits in primary visual cortex of the macaque monkey. Annu. Rev. Neurosci. 21, 47–74 (1998).

    Article  CAS  Google Scholar 

  2. 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 

  3. Lund, J.S., Henry, G.H., MacQueen, C.L. & Harvey, A.R. Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey. J. Comp. Neurol. 184, 599–618 (1979).

    Article  CAS  Google Scholar 

  4. Binzegger, T., Douglas, R.J. & Martin, K.A. A quantitative map of the circuit of cat primary visual cortex. J. Neurosci. 24, 8441–8453 (2004).

    Article  CAS  Google Scholar 

  5. Brecht, M., Roth, A. & Sakmann, B. Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex. J. Physiol. (Lond.) 553, 243–265 (2003).

    Article  CAS  Google Scholar 

  6. Brumberg, J.C., Pinto, D.J. & Simons, D.J. Cortical columnar processing in the rat whisker-to-barrel system. J. Neurophysiol. 82, 1808–1817 (1999).

    Article  CAS  Google Scholar 

  7. Bullier, J. & Henry, G.H. Ordinal position of neurons in cat striate cortex. J. Neurophysiol. 42, 1251–1263 (1979).

    Article  CAS  Google Scholar 

  8. Contreras, D. & Palmer, L.A. Response to contrast of electrophysiologically defined cell classes in primary visual cortex. J. Neurosci. 23, 6936–6945 (2003).

    Article  CAS  Google Scholar 

  9. Gilbert, C.D. Laminar differences in receptive field properties of cells in cat primary visual cortex. J. Physiol. (Lond.) 268, 391–421 (1977).

    Article  CAS  Google Scholar 

  10. Gilbert, C.D. & Wiesel, T.N. Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280, 120–125 (1979).

    Article  CAS  Google Scholar 

  11. Hirsch, J.A. et al. Synaptic physiology of the flow of information in the cat's visual cortex in vivo. J. Physiol. (Lond.) 540, 335–350 (2002).

    Article  CAS  Google Scholar 

  12. Hubel, D.H. & Wiesel, T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962).

    Article  CAS  Google Scholar 

  13. Kagan, I., Gur, M. & Snodderly, D.M. Spatial organization of receptive fields of V1 neurons of alert monkeys: comparison with responses to gratings. J. Neurophysiol. 88, 2557–2574 (2002).

    Article  Google Scholar 

  14. Linden, J.F. & Schreiner, C.E. Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. Cereb. Cortex 13, 83–89 (2003).

    Article  Google Scholar 

  15. Martin, K.A. & Whitteridge, D. Form, function and intracortical projections of spiny neurons in the striate visual cortex of the cat. J. Physiol. (Lond.) 353, 463–504 (1984).

    Article  CAS  Google Scholar 

  16. Martinez, L.M., Alonso, J.M., Reid, R.C. & Hirsch, J.A. Laminar processing of stimulus orientation in cat visual cortex. J. Physiol. 540, 321–333 (2002).

    Article  CAS  Google Scholar 

  17. Mooser, F., Bosking, W.H. & Fitzpatrick, D. A morphological basis for orientation tuning in primary visual cortex. Nat. Neurosci. 8, 872–879 (2004).

    Article  Google Scholar 

  18. Nowak, L.G., Azouz, R., Sanchez-Vives, M.V., Gray, C.M. & McCormick, D.A. Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. J. Neurophysiol. 89, 1541–1566 (2003).

    Article  Google Scholar 

  19. Swadlow, H.A. & Hicks, T.P. Somatosensory cortical efferent neurons of the awake rabbit: latencies to activation via supra- and subthreshold receptive fields. J. Neurophysiol. 75, 1753–1759 (1996).

    Article  CAS  Google Scholar 

  20. Ringach, D.L., Shapley, R. & Hawken, M.J. Orientation selectivity in macaque V1: diversity and laminar dependence. J. Neurosci. 22, 5639–5651 (2002).

    Article  CAS  Google Scholar 

  21. Jones, J.P. & Palmer, L.A. The two-dimensional spatial structure of simple receptive fields in cat striate cortex. J. Neurophysiol. 58, 1187–1211 (1987).

    Article  CAS  Google Scholar 

  22. Palmer, L.A. & Davis, T.L. Receptive-field structure in cat striate cortex. J. Neurophysiol. 46, 260–276 (1981).

    Article  CAS  Google Scholar 

  23. Ferster, D. Spatially opponent excitation and inhibition in simple cells of the cat visual cortex. J. Neurosci. 8, 1172–1180 (1988).

    Article  CAS  Google Scholar 

  24. Chapman, B., Zahs, K.R. & Stryker, M.P. Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. J. Neurosci. 11, 1347–1358 (1991).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  26. Ferster, D. & Miller, K.D. Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23, 441–471 (2000).

    Article  CAS  Google Scholar 

  27. Chance, F.S., Nelson, S.B. & Abbott, L.F. Complex cells as cortically amplified simple cells. Nat. Neurosci. 2, 277–282 (1999).

    Article  CAS  Google Scholar 

  28. Borg-Graham, L.J., Monier, C. & Fregnac, Y. Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393, 369–373 (1998).

    Article  CAS  Google Scholar 

  29. Mata, M.L. & Ringach, D.L. Spatial overlap of On and Off subregions and its relation to response modulation ratio in macaque primary visual cortex. J. Neurophysiol. (in the press).

  30. Rivadulla, C., Sharma, J. & Sur, M. Specific roles of NMDA and AMPA receptors in direction-selective and spatial phase-selective responses in visual cortex. J. Neurosci. 21, 1710–1719 (2001).

    Article  CAS  Google Scholar 

  31. Tao, L., Shelley, M., McLaughlin, D. & Shapley, R. An egalitarian network model for the emergence of simple and complex cells in visual cortex. Proc. Natl. Acad. Sci. USA 101, 366–371 (2004).

    Article  CAS  Google Scholar 

  32. Priebe, N.J., Mechler, F., Carandini, M. & Ferster, D. The contribution of spike threshold to the dichotomy of cortical simple and complex cells. Nat. Neurosci. 7, 1113–1122 (2004).

    Article  CAS  Google Scholar 

  33. Schiller, P.H., Finlay, B.L. & Volman, S.F. Quantitative studies of single-cell properties in monkey striate cortex. I. Spatiotemporal organization of receptive fields. J. Neurophysiol. 39, 1288–1319 (1976).

    Article  CAS  Google Scholar 

  34. De Angelis, G.C., Ohzawa, I. & Freeman, R.D. Receptive field dynamics in central visual pathways. Trends Neurosci. 18, 451–458 (1995).

    Article  CAS  Google Scholar 

  35. Hirsch, J.A., Alonso, J.M., Reid, R.C. & Martinez, L.M. Synaptic integration in striate cortical simple cells. J. Neurosci. 18, 9517–9528 (1998).

    Article  CAS  Google Scholar 

  36. Hirsch, J.A. et al. Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat. Neurosci. 6, 1300–1308 (2003).

    Article  CAS  Google Scholar 

  37. Lauritzen, T.Z. & Miller, K.D. Different roles for simple- and complex-cell inhibition in V1. J. Neurosci. 23, 10201–10213 (2003).

    Article  CAS  Google Scholar 

  38. Dean, A.F. & Tolhurst, D.J. On the distinctness of simple and complex cells in the visual cortex of the cat. J. Physiol. (Lond.) 344, 305–325 (1983).

    Article  CAS  Google Scholar 

  39. Grieve, K.L. & Sillito, A.M. A re-appraisal of the role of layer VI of the visual cortex in the generation of cortical end inhibition. Exp. Brain Res. 87, 521–529 (1991).

    Article  CAS  Google Scholar 

  40. Hirsch, J.A., Gallagher, C.A., Alonso, J.M. & Martinez, L.M. Ascending projections of simple and complex cells in layer 6 of the cat striate cortex. J. Neurosci. 18, 8086–8094 (1998).

    Article  CAS  Google Scholar 

  41. Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J. Physiol. (Lond.) 283, 53–77 (1978a).

    Article  CAS  Google Scholar 

  42. Troyer, T.W., Krukowski, A.E., Priebe, N.J. & Miller, K.D. Contrast-invariant orientation tuning in cat visual cortex: thalamocortical input tuning and correlation-based intracortical connectivity. J. Neurosci. 18, 5908–5927 (1998).

    Article  CAS  Google Scholar 

  43. Usrey, W.M., Sceniak, M.P. & Chapman, B. Receptive fields and response properties of neurons in layer 4 of ferret visual cortex. J. Neurophysiol. 89, 1003–1015 (2003).

    Article  Google Scholar 

  44. Bullier, J. & Henry, G.H. Ordinal position and afferent input of neurons in monkey striate cortex. J. Comp. Neurol. 193, 913–935 (1980).

    Article  CAS  Google Scholar 

  45. Henry, G.H. Receptive field classes of cells in the striate cortex of the cat. Brain Res. 133, 1–28 (1977).

    Article  CAS  Google Scholar 

  46. Toyama, K., Kimura, M. & Tanaka, K. Organization of cat visual cortex as investigated by cross-correlation analysis. J. Neurophysiol. 46, 202–214 (1981).

    Article  CAS  Google Scholar 

  47. Skottun, B.C. et al. Classifying simple and complex cells on the basis of response modulation. Vision Res. 31, 1079–1086 (1991).

    CAS  PubMed  Google Scholar 

  48. Mechler, F. & Ringach, D.L. On the classification of simple and complex cells. Vision Res. 42, 1017–1033 (2002).

    Article  Google Scholar 

  49. Chisum, H.J., Mooser, F. & Fitzpatrick, D. Emergent properties of layer 2/3 neurons reflect the collinear arrangement of horizontal connections in tree shrew visual cortex. J. Neurosci. 23, 2947–2960 (2003).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank T.N. Wiesel for support over the years and C.G. Marshall, K.D. Naik and J.M. Provost for assistance with the anatomical reconstructions. Supported by US National Institutes of Health grant EY09593 to J.A.H.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Judith A Hirsch.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Martinez, L., Wang, Q., Reid, R. et al. Receptive field structure varies with layer in the primary visual cortex. Nat Neurosci 8, 372–379 (2005). https://doi.org/10.1038/nn1404

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1404

This article is cited by

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