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Functionally distinct inhibitory neurons at the first stage of visual cortical processing

Nature Neuroscience volume 6, pages 1300–1308 (2003)Cite this article

Abstract

Here we explore inhibitory circuits at the thalamocortical stage of processing in layer 4 of the cat's visual cortex, focusing on the anatomy and physiology of the interneurons themselves. Our immediate aim was to explore the inhibitory mechanisms that contribute to orientation selectivity, perhaps the most dramatic response property to emerge across the thalamocortical synapse. The broader goal was to understand how inhibitory circuits operate. Using whole-cell recording in cats in vivo, we found that layer 4 contains two populations of inhibitory cells defined by receptive field class—simple and complex. The simple cells were selective for stimulus orientation, whereas the complex cells were not. Our observations help to explain how neurons become sensitive to stimulus orientation and maintain that selectivity as stimulus contrast changes. Overall, the work suggests that different sources of inhibition, either selective for specific features or broadly tuned, interact to provide appropriate representations of elements within the environment.

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Figure 8: Summary of results.
Figure 1: Morphology of smooth cells with simple receptive fields.
Figure 2: The receptive fields of smooth and spiny simple cells look alike.
Figure 3: Push-pull structure of the smooth simple cell receptive field.
Figure 4: Smooth simple cells are orientation-selective.
Figure 5: Morphology of smooth cells with complex receptive fields.
Figure 6: Push-push structure of the complex smooth cell receptive field.
Figure 7: Smooth complex cells are not orientation-selective.

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References

  1. Martin, K.A., Somogyi, P. & Whitteridge, D. Physiological and morphological properties of identified basket cells in the cat's visual cortex. Exp. Brain Res. 50, 193–200 (1983).

    CAS  PubMed  Google Scholar 

  2. Azouz, R., Gray, C.M., Nowak, L.G. & McCormick, D.A. Physiological properties of inhibitory interneurons in cat striate cortex. Cereb. Cortex 7, 534–545 (1997).

    Article  CAS  PubMed  Google Scholar 

  3. Buzas, P., Eysel, U.T., Adorjan, P. & Kisvarday, Z.F. Axonal topography of cortical basket cells in relation to orientation, direction, and ocular dominance maps. J. Comp. Neurol. 437, 259–285 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Thomson, A.M. & West, D.C. Presynaptic frequency filtering in the gamma frequency band; dual intracellular recordings in slices of adult rat and cat neocortex. Cereb. Cortex 13, 136–143 (2003).

    Article  PubMed  Google Scholar 

  5. 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 

  6. Sclar, G. & Freeman, R.D. Orientation selectivity in the cat's striate cortex is invariant with stimulus contrast. Exp. Brain Res. 46, 457–461 (1982).

    Article  CAS  PubMed  Google Scholar 

  7. Ohzawa, I., Sclar, G. & Freeman, R.D. Contrast gain control in the cat's visual system. J. Neurophysiol. 54, 651–667 (1985).

    Article  CAS  PubMed  Google Scholar 

  8. Bruno, R.M. & Simons, D.J. Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J. Neurosci. 22, 10966–10975 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Swadlow, H.A. & Gusev, A.G. Receptive-field construction in cortical inhibitory interneurons. Nat. Neurosci. 5, 403–404 (2002).

    Article  CAS  PubMed  Google Scholar 

  10. Swadlow, H.A. Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb. Cortex 13, 25–32 (2003).

    Article  PubMed  Google Scholar 

  11. 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  PubMed  Google Scholar 

  12. Gabbott, P.L. & Somogyi, P. Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat. Exp. Brain Res. 61, 323–331 (1986).

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  14. 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 

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

    Article  CAS  PubMed  Google Scholar 

  16. Tanaka, K. Organization of geniculate inputs to visual cortical cells in the cat. Vision Res. 25, 357–364 (1985).

    Article  CAS  PubMed  Google Scholar 

  17. 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  PubMed  Google Scholar 

  18. Ferster, D. Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. J. Neurosci. 6, 1284–1301 (1986).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  20. 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 

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

    Article  CAS  PubMed  Google Scholar 

  22. 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  PubMed  PubMed Central  Google Scholar 

  23. 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  PubMed  Google Scholar 

  24. Wielaard, D.J., Shelley, M., McLaughlin, D. & Shapley, R. How simple cells are made in a nonlinear network model of the visual cortex. J. Neurosci. 21, 5203–5211 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Monier, C., Chavane, F., Baudot, P., Borg-Graham, L.J. & Fregnac, Y. Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37, 663–680 (2003).

    Article  CAS  PubMed  Google Scholar 

  26. Burr, D., Morrone, C. & Maffei, L. Intra-cortical inhibition prevents simple cells from responding to textured visual patterns. Exp. Brain Res. 43, 455–458 (1981).

    CAS  PubMed  Google Scholar 

  27. Sillito, A.M. GABA mediated inhibitory processes in the function of the geniculo-striate system. Prog. Brain Res. 90, 349–384 (1992).

    Article  CAS  PubMed  Google Scholar 

  28. Somers, D.C., Nelson, S.B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448–5465 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 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  PubMed  PubMed Central  Google Scholar 

  30. Ringach, D.L., Hawken, M.J. & Shapley, R. Dynamics of orientation tuning in macaque V1: the role of global and tuned supression. J. Neurophysiol. 90, 342–352 (2003).

    Article  PubMed  Google Scholar 

  31. Troyer, T.W., Krukowski, A.E. & Miller, K.D. LGN input to simple cells and contrast-invariant orientation tuning: an analysis. J. Neurophysiol. 87, 2741–2752 (2002).

    Article  PubMed  Google Scholar 

  32. Lauritzen, T.Z. & Miller, K.D. Different roles for simple- and complex-cell inhibition in V1. J. Neurosci. (in press).

  33. 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  PubMed  Google Scholar 

  34. Hirsch, J.A. Synaptic integration in layer IV of the ferret striate cortex. J. Physiol. (Lond.) 483, 183–199 (1995).

    Article  CAS  Google Scholar 

  35. Gibson, J.R., Beierlein, M. & Connors, B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75–79 (1999).

    Article  CAS  PubMed  Google Scholar 

  36. Porter, J.T., Johnson, C.K. & Agmon, A. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J. Neurosci. 21, 2699–2710 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

  38. Hirsch, J.A. Synaptic physiology and receptive field structure in the early visual pathway of the cat. Cereb. Cortex 13, 63–69 (2003).

    Article  PubMed  Google Scholar 

  39. 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  PubMed  Google Scholar 

  40. Anderson, J., Carandini, M. & Ferster, D. Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J. Neurophysiol. 84, 909–926 (2000).

    Article  CAS  PubMed  Google Scholar 

  41. Kayser, A.S. & Miller, K.D. Opponent inhibition: a developmental model of layer 4 of the neocortical circuit. Neuron 33, 131–142 (2002).

    Article  CAS  PubMed  Google Scholar 

  42. Volgushev, M., Pei, X., Vidyasagar, T.R. & Creutzfeldt, O.D. Excitation and inhibition in orientation selectivity of cat visual cortex neurons revealed by whole-cell recordings in vivo. Vis. Neurosci. 10, 1151–1155 (1993).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  44. 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  PubMed  Google Scholar 

  45. 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  PubMed  PubMed Central  Google Scholar 

  46. Carandini, M., Heeger, D.J. & Senn, W. A synaptic explanation of suppression in visual cortex. J. Neurosci. 22, 10053–10065 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. 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  PubMed  Google Scholar 

  48. Moore, C.I., Nelson, S.B. & Sur, M. Dynamics of neuronal processing in rat somatosensory cortex. Trends Neurosci. 22, 513–520 (1999).

    Article  CAS  PubMed  Google Scholar 

  49. 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 

  50. 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 

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Acknowledgements

We thank T.N. Wiesel for discussions, K.D. Miller for improving the manuscript, R.C. Reid for contributing software and C.G. Marshall, K.D. Naik and J.M. Provost for assistance with the reconstructions. Supported by National Institutes of Health EY09593 to J.A.H.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Southern California, 3641 Watt Way, Los Angeles, 90089-2520, California, USA

    Judith A Hirsch, Cinthi Pillai & Qingbo Wang

  2. Department of Medicine, Campus de Oza, Universidad A Coruña, 15006, Spain

    Luis M Martinez

  3. Department of Biological Sciences, SUNY-Optometry, 33 West 42nd Street, New York, 10036, New York, USA

    Jose-Manuel Alonso

  4. Redwood Neuroscience Institute, 1010 El Camino Real, Menlo Park, 94025, California, USA

    Friedrich T Sommer

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Correspondence to Judith A Hirsch.

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Supplementary information

Supplementary Fig. 1.

Responses to oriented bars for three additional simple and three additional complex cells. Each panel in a-f shows results from a single interneuron; simple cells (a-c), complex cells (d-f). For every cell, a contour plot of the receptive field is shown above averaged responses to variously oriented moving bars. In each column of records, the top trace depicts the response evoked by an optimally oriented bar; subsequent records show responses to bars tilted 22, 45, and 90° away from the preferred orientation. For the simple cell of panel a, an optimally oriented dark bar evoked a pattern of depolarization, hyperpolarization and depolarization as it crossed the Off, On and Off subregions. The response was similar at the near preferred angle and then diminished as the stimulus tilted towards the orthogonal orientation; similar patterns were seen in c for a cell whose receptive field also had three subregions. The records shown in b are from a cell whose receptive field has just two subregions. As a bright bar coursed over the On and Off subregions it first elicited a depolarization, then a hyperpolarization and finally a second depolarization on exit from the receptive field. For complex cells, (d-f), responses to the moving bars were similar at all orientations. Scale bars are 5 mV and 200 msec; all conventions as for figures in the text. A plot of the tuning curves for depolarization for all cells is shown in g; gray lines indicate curves for complex cells and black lines curves for simple cells. (JPG 43 kb)

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Hirsch, J., Martinez, L., Pillai, C. et al. Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat Neurosci 6, 1300–1308 (2003). https://doi.org/10.1038/nn1152

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