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Functional connectivity between simple cells and complex cells in cat striate cortex

Nature Neuroscience volume 1, pages 395–403 (1998)Cite this article

Abstract

In the cat primary visual cortex, neurons are classified into the two main categories of simple cells and complex cells based on their response properties. According to the hierarchical model, complex receptive fields derive from convergent inputs of simple cells with similar orientation preferences. This model received strong support from anatomical studies showing that many complex cells lie within the range of layer IV simple-cell axons but outside the range of most thalamic axons. Physiological evidence for the model, however, has remained elusive. Here we demonstrate that layer IV simple cells and layer II and III complex cells show correlated firing consistent with monosynaptic connections. As expected from the hierarchical model, all connections were in the direction from the simple cell to the complex cell, most frequently between cells with similar orientation preferences.

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Figure 1: Coronal section (thickness, 40 μm) of cat visual cortex showing five electrode tracks in the medial bank.
Figure 2: A layer IV simple cell simultaneously recorded with a layer II complex cell.
Figure 3: A layer IV simple cell simultaneously recorded with a complex cell located near the layer III/IV border.
Figure 4: A layer IV simple cell simultaneously recorded with a layer III complex cell.
Figure 5: Distribution of correlations between simple cells and complex cells according to their symmetry with respect to zero.
Figure 6: Complex cells with asymmetric correlograms were usually located superficially in the cortex and were not correlated with layer A geniculate multi-unit activity.
Figure 7: Convergence of layer IV simple cells and layer III/IV border complex cells onto layer II and III complex cells.
Figure 8: Four different circuits that could make a simple cell fire before a complex cell.

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References

  1. 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 

  2. 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 

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

    Article  CAS  Google Scholar 

  4. Ferster, D., Chung, S. & Wheat, H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249–252 (1996).

    Article  CAS  Google Scholar 

  5. Sompolinsky H. Shapley R. New perspectives on the mechanisms for orientation selectivity. Curr. Opin. Neurobiol. 7, 514–522 (1997).

    Article  CAS  Google Scholar 

  6. Toyama, K., Kimura, M. & Tanaka, K. Cross-correlation analysis of interneuronal connectivity in cat visual cortex. J. Neurophysiol. 46, 191–201 (1981).

    Article  CAS  Google Scholar 

  7. 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 

  8. Ghose, G. M., Freeman, R. D. & Ozhawa, I. Local intracortical connections in the cat's visual cortex: postnatal development and plasticity. J. Neurophysiol. 72, 1290–1303 (1994).

    Article  CAS  Google Scholar 

  9. Hoffman, K. P. & Stone, J. Conduction velocity of afferents of cat visual cortex: a correlation with cortical receptive field properties. Brain Res. 32, 460–466 (1971).

    Article  CAS  Google Scholar 

  10. Bullier J. & Henry, G. H. Laminar distribution of first order neurons and afferent terminals in cat striate cortex. J. Neurophysiol. 42, 1271–1281 (1979).

    Article  CAS  Google Scholar 

  11. Ferster, D. & Lindstrom, S. An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat. J. Physiol. (Lond.) 342, 181–215 (1983).

    Article  CAS  Google Scholar 

  12. Tanaka, K. Cross-correlation analysis of geniculostriate neuronal relationships in the cat. J. Neurophysiol. 49, 1303–1318 (1983).

    Article  CAS  Google Scholar 

  13. Martin, K. A. C. & 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 

  14. Heggelund, P. Receptive field organization of complex cells in cat striate cortex. Exp. Brain. Res. 42, 99–107 (1981).

    Google Scholar 

  15. Mel, B. W., Ruderman, D. L. & Archie, K. A. Translation-invariant orientation tuning in visual complex cells could derive from intradendritic computations. J. Neurosci. 18, 4325–4334 (1998).

    Article  CAS  Google Scholar 

  16. Hammond, P. & MacKay, D. M. Differential responsiveness of simple and complex cells in cat striate cortex to visual texture. Exp. Brain Res. 30, 275–296 (1977).

    CAS  Google Scholar 

  17. Malpeli, J. G. Activity of cells in area 17 of the cat in absence of input from layer A of lateral geniculate nucleus. J. Neurophysiol. 49, 595–610 (1983).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  19. 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 

  20. Hirsch, J. A., Alonso, J. M. & Reid, R. C. Visually evoked calcium action potentials in cat striate cortex. Nature 378, 612–616 (1995).

    Article  CAS  Google Scholar 

  21. 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 

  22. Orban, G. A. Neuronal Operations in the Visual Cortex. (Springer-Verlag, Berlin, 1984).

    Book  Google Scholar 

  23. Movshon J., Thompson I. & Tolhurst D. Receptive field organization of complex cells in cat's striate cortex. J. Physiol. (Lond.) 283, 79–99 (1978).

    Article  CAS  Google Scholar 

  24. Adelson, E. H. & Bergen, J. R. Spationtemporal energy models for the perception of motion. J. Opt. Soc. Am. A2, 284–299 (1985).

    Article  Google Scholar 

  25. Ohzawa, I., DeAngelis, G. C. & Freeman, R. D. Stereoscopic depth discrimination in the visual cortex: neurons ideally suited as disparity detectors. Science 249, 1037–1041 (1990).

    Article  CAS  Google Scholar 

  26. Heeger, D. J. Normalization of cell responses in cat striate cortex. Visual Neurosci. 9, 181–197 (1992).

    Article  CAS  Google Scholar 

  27. Eckhorn, R. & Thomas, U. Guidance of thin-shaft microprobes by rubber tubes: a new method for the insertion of multiple microprobes into neuronal and muscular tissue, including fiber-electrodes, fine wires, needles and microsensors. J. Neurosci. Methods. 49, 175–185 (1993).

    Article  CAS  Google Scholar 

  28. Snodderly D. M. & Gur, M. Organization of striate cortex of alert, trained monkeys (Macaca fascicularis): ongoing activity, stimulus selectivity, and widths of receptive field activating regions. J. Neurophysiol. 74, 2100–2125 (1995).

    Article  CAS  Google Scholar 

  29. Sutter, E. in Advanced Methods of Physiological Systems Modeling Vol. 1, 303–315 (Univ. Southern California, 1987 ).

    Google Scholar 

  30. Reid, R. C., Victor, J. D. & Shapley, R. M. The use of m-sequences in the analysis of visual neurons: linear receptive field properties. Visual Neurosci. 14, 1015–1027 (1997).

    Article  CAS  Google Scholar 

  31. Moore, G. P., Segundo, J. P., Perkel, D. H. & Levitan, H. Statistical signs of synaptic interaction in neurons. Biophys. J. 10, 876–900 (1970).

    Article  CAS  Google Scholar 

  32. Perkel, D. H., Gerstein, G. L. & Moore, G. P. Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys. J. 7, 419–440 (1967).

    Article  CAS  Google Scholar 

  33. 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 

  34. Alonso, J. M., Usrey, W. M. & Reid, R. C. Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383, 815–819 (1996).

    Article  CAS  Google Scholar 

  35. Fetz, E. E. & Gustafsson, B. Relation between shapes of post-synaptic potentials and changes in firing probability of cat motoneurons. J. Physiol. (Lond.) 341, 387–410 (1983).

    Article  CAS  Google Scholar 

  36. Surmeier, D. J. & Weinberg, R. J. The relationship between cross-correlation measures and underlying synaptic events. Brain Res. 331, 180–184 (1985).

    Article  CAS  Google Scholar 

  37. Matsumura, M., Chen, D., Sawaguchi, T., Kubota, K. & Fetz, E. E. Synaptic interactions between primate precentral cortex neurons revealed by spike-triggered averaging of intracellular membrane potentials in vivo. J. Neurosci. 23, 7757–7767 (1996).

    Article  Google Scholar 

  38. 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 

  39. Sillito, A. M. Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex. J. Physiol.(Lond.) 271, 699–720 (1977).

    Article  CAS  Google Scholar 

  40. Markram, H., Lubke, J., Frotscher, M., Roth, A. & Sakmann, B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J. Physiol. (Lond.) 500, 409–440 (1997).

    Article  CAS  Google Scholar 

  41. Stratford, K. J., Tarczy-Hornoch, K., Martin, K. A. C., Bannister, N. J. & Jack J. J. B Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature 382, 258–261 (1996).

    Article  CAS  Google Scholar 

  42. Deuchars, J., West, D. C. & Thomson, A. M. Relationships between morphology and physiology of pyramid-pyramid single axon connections in rat neocortex in vitro. J. Physiol. (Lond.) 478, 423–435 (1994).

    Article  Google Scholar 

  43. Mason, A., Nicoll, A. & Stratford, K. Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro. J. Neurosci. 11, 72–84 (1991).

    Article  CAS  Google Scholar 

  44. Ferster, D. & Lindstrom, S. Synaptic excitation of neurons in area 17 of the cat by intracortical axon collaterals of cortico-geniculate cells. J. Physiol. (Lond.) 367, 233–252 (1985).

    Article  CAS  Google Scholar 

  45. Fitzsimonds, R. M., Song, H. J. & Poo, M. M. Propagation of activity-dependent synaptic depression in simple neural networks. Nature 388, 439–448 (1997).

    Article  CAS  Google Scholar 

  46. Singer, W., Tretter, F. & Cynader, M. Organization of cat striate cortex: a correlation of receptive-field properties with afferent and efferent connections. J. Neurophysiol. 38, 1080–1098 (1975).

    Article  CAS  Google Scholar 

  47. Kirkwood, P. A. On the use and interpretation of cross-correlation measurements in the mammalian central nervous system. J. Neurosci. Methods 1, 107–132 (1979).

    Article  CAS  Google Scholar 

  48. Sherman, S. M. & Guillery, R. W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367–1395 (1996).

    Article  CAS  Google Scholar 

  49. Humphrey, A. L., Sur, M., Uhlrich, D. J. & Sherman, S. M. Projection patterns of individual X- and Y-cell axons from the lateral geniculate nucleus to cortical area 17 in the cat. J. Comp Neurol. 233, 159–189 (1985).

    Article  CAS  Google Scholar 

  50. Ts'o, D. Y., Gilbert C. D. & Wiesel T. N. Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J. Neurosci. 6, 1160–1170 (1986).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank T.N. Wiesel for discussion and suggestions. We also thank C. Reid, D. Ferster, R. Freeman and J. Hirsch for criticisms and comments. Technical assistance was provided by K. Desai, J. Kornblum, and K. McGowan. Thanks to Sonia and Claudia. This study was supported by the NIH and Human Frontier Science Program Organization.

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    1. Laboratory of Neurobiology, The Rockefeller University, New York, 10021, New York, USA

      Jose-Manuel Alonso & Luis M. Martinez

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    Correspondence to Jose-Manuel Alonso.

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    Alonso, JM., Martinez, L. Functional connectivity between simple cells and complex cells in cat striate cortex. Nat Neurosci 1, 395–403 (1998). https://doi.org/10.1038/1609

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