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
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Callaway, E.M. Local circuits in primary visual cortex of the macaque monkey. Annu. Rev. Neurosci. 21, 47–74 (1998).
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).
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).
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).
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).
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).
Bullier, J. & Henry, G.H. Ordinal position of neurons in cat striate cortex. J. Neurophysiol. 42, 1251–1263 (1979).
Contreras, D. & Palmer, L.A. Response to contrast of electrophysiologically defined cell classes in primary visual cortex. J. Neurosci. 23, 6936–6945 (2003).
Gilbert, C.D. Laminar differences in receptive field properties of cells in cat primary visual cortex. J. Physiol. (Lond.) 268, 391–421 (1977).
Gilbert, C.D. & Wiesel, T.N. Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280, 120–125 (1979).
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).
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).
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).
Linden, J.F. & Schreiner, C.E. Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. Cereb. Cortex 13, 83–89 (2003).
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).
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).
Mooser, F., Bosking, W.H. & Fitzpatrick, D. A morphological basis for orientation tuning in primary visual cortex. Nat. Neurosci. 8, 872–879 (2004).
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).
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).
Ringach, D.L., Shapley, R. & Hawken, M.J. Orientation selectivity in macaque V1: diversity and laminar dependence. J. Neurosci. 22, 5639–5651 (2002).
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).
Palmer, L.A. & Davis, T.L. Receptive-field structure in cat striate cortex. J. Neurophysiol. 46, 260–276 (1981).
Ferster, D. Spatially opponent excitation and inhibition in simple cells of the cat visual cortex. J. Neurosci. 8, 1172–1180 (1988).
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).
Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).
Ferster, D. & Miller, K.D. Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23, 441–471 (2000).
Chance, F.S., Nelson, S.B. & Abbott, L.F. Complex cells as cortically amplified simple cells. Nat. Neurosci. 2, 277–282 (1999).
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).
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).
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).
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).
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).
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).
De Angelis, G.C., Ohzawa, I. & Freeman, R.D. Receptive field dynamics in central visual pathways. Trends Neurosci. 18, 451–458 (1995).
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).
Hirsch, J.A. et al. Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat. Neurosci. 6, 1300–1308 (2003).
Lauritzen, T.Z. & Miller, K.D. Different roles for simple- and complex-cell inhibition in V1. J. Neurosci. 23, 10201–10213 (2003).
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).
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).
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).
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).
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).
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).
Bullier, J. & Henry, G.H. Ordinal position and afferent input of neurons in monkey striate cortex. J. Comp. Neurol. 193, 913–935 (1980).
Henry, G.H. Receptive field classes of cells in the striate cortex of the cat. Brain Res. 133, 1–28 (1977).
Toyama, K., Kimura, M. & Tanaka, K. Organization of cat visual cortex as investigated by cross-correlation analysis. J. Neurophysiol. 46, 202–214 (1981).
Skottun, B.C. et al. Classifying simple and complex cells on the basis of response modulation. Vision Res. 31, 1079–1086 (1991).
Mechler, F. & Ringach, D.L. On the classification of simple and complex cells. Vision Res. 42, 1017–1033 (2002).
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).
Diamond, M.E., Huang, W. & Ebner, F.F. Laminar comparison of somatosensory cortical plasticity. Science 265, 1885–1888 (1994).
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
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn1404
This article is cited by
-
Perirhinal circuits for memory processing
Nature Reviews Neuroscience (2019)
-
An open repository for single-cell reconstructions of the brain forest
Scientific Data (2018)
-
Principles underlying sensory map topography in primary visual cortex
Nature (2016)
-
Columnar organization of spatial phase in visual cortex
Nature Neuroscience (2015)
-
Spatiotemporal receptive fields of barrel cortex revealed by reverse correlation of synaptic input
Nature Neuroscience (2014)