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Contrast's effect on spatial summation by macaque V1 neurons

Abstract

Stimulation outside the receptive field of a primary visual cortical (V1) neuron reveals intracortical neural interactions1,2,3,4,5,6. However, previous investigators implicitly or explicitly considered the extent of cortical spatial summation and, therefore, the size of the classical receptive field to be fixed and independent of stimulus characteristics or of surrounding context. On the contrary, we found that the extent of spatial summation in macaque V1 neurons depended on contrast, and was on average 2.3-fold greater at low contrast. This adaptive increase in spatial summation at low contrast was seen in cells throughout V1 and was independent of surround inhibition.

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Figure 1: Spatial summation responses for three V1 neurons.
Figure 2: Difference of Gaussians model for cortical receptive fields.
Figure 3: Dependence of excitatory spread on stimulus contrast.
Figure 4: Comparison of contrast-dependent change in excitatory space constant, a, and optimal radius.
Figure 5: Laminar distribution of changes in excitatory space constant with contrast.
Figure 6: Changes in surround strength with contrast.
Figure 7: Cells which show no surround suppression at either contrast.

References

  1. Maffei, L. & Fiorentini, A. The unresponsive regions of visual cortical receptive fields. Vision Res. 16, 1131–1139 (1976).

    Article  CAS  Google Scholar 

  2. Nelson, J. I. & Frost, B. J. Orientation-selective inhibition from beyond the classic visual receptive field. Brain Res. 139, 359–365 (1978).

    Article  CAS  Google Scholar 

  3. Allman, J., Miezin, F. & McGuinness, E. Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. Annu. Rev. Neurosci. 8, 407–430 (1985).

    Article  CAS  Google Scholar 

  4. Levitt, J. B. & Lund, J. S. Contrast dependence of contextual effects in primate visual cortex. Nature 387, 73–76 (1997).

    Article  CAS  Google Scholar 

  5. Polat, U., Mizobe, K., Pettet, M. W., Kasamatsu, T. & Norcia, A. M. Collinear stimuli regulate visual responses depending on cell's contrast threshold. Nature 391, 580–584 (1998).

    Article  CAS  Google Scholar 

  6. Kapadia, M. K., Ito, M., Gilbert, C. D. & Westheimer, G. Improvement in visual sensitivity by changes in local context: parallel studies in human observers and in V1 of alert monkeys. Neuron 15, 843–856 (1995).

    Article  CAS  Google Scholar 

  7. Zipser, K., Lamme, V. A. & Schiller, P. H. Contextual modulation in primary visual cortex. J. Neurosci. 16, 7376–7389 (1996).

    Article  CAS  Google Scholar 

  8. Somers, D. C. et al. A local circuit approach to understanding integration of long-range inputs in primary visual cortex. Cereb. Cortex 8, 204–217 (1998).

    Article  CAS  Google Scholar 

  9. Rodieck, R. W. Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res. 5, 583–601 (1965).

    Article  CAS  Google Scholar 

  10. Enroth-Cugell, C. & Robson, J. G. The contrast sensitivity of retinal ganglion cells of the cat. J. Physiol. (Lond.) 187, 517–552 ( 1966).

    Article  CAS  Google Scholar 

  11. DeAngelis, G. C., Freeman, R. D. & Ohzawa, I. Length and width tuning of neurons in the cat's primary visual cortex. J. Neurophysiol. 71, 347– 374 (1994).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Bonds, A. B. Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Vis. Neurosci. 2, 41–55 (1989).

    Article  CAS  Google Scholar 

  14. Sillito, A. M., Grieve, K. L., Jones, H. E., Cudeiro, J. & Davis, J. Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378, 492–496 (1995).

    Article  CAS  Google Scholar 

  15. Hawken, M. J., Parker, A. J. & Lund, J. S. Laminar organization and contrast sensitivity of direction- selective cells in the striate cortex of the Old World monkey. J. Neurosci. 8, 3541–3548 (1988).

    Article  CAS  Google Scholar 

  16. Pettet, M. W. & Gilbert, C. D. Dynamic changes in receptive-field size in cat primary visual cortex. Proc. Natl. Acad. Sci. USA 89, 8366–8370 (1992).

    Article  CAS  Google Scholar 

  17. DeAngelis, G. C., Anzai, A., Ohzawa, I. & Freeman, R. D. Receptive field structure in the visual cortex: does selective stimulation induce plasticity? Proc. Natl. Acad. Sci. USA 92, 9682– 9686 (1995).

    Article  CAS  Google Scholar 

  18. Sengpiel, F., Sen, A. & Blakemore, C. Characteristics of surround inhibition in cat area 17. Exp. Brain Res. 116, 216– 228 (1997).

    Article  CAS  Google Scholar 

  19. Markram, H. & Tsodyks, M. Redistribution of synaptic efficacy: a mechanism to generate infinite synaptic input diversity from a homogeneous population of neurons without changing absolute synaptic efficacies. J. Physiol. (Paris) 90, 229–232 (1996).

    Article  CAS  Google Scholar 

  20. Thomson, A. M. Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J. Physiol. (Lond.) 502, 131–147 ( 1997).

    Article  CAS  Google Scholar 

  21. Thomson, A. M. & Deuchars, J. Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb. Cortex 7, 510–522 (1997).

    Article  CAS  Google Scholar 

  22. Bernander, O., Douglas, R. J., Martin, K. A. & Koch, C. Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc. Natl. Acad. Sci. USA 88, 11569–11573 (1991).

    Article  CAS  Google Scholar 

  23. Häusser, M. & Clark, B. A. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665–678 (1997).

    Article  Google Scholar 

  24. 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 

  25. Borg, G. J., Monier, C. & Frégnac, Y. Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393, 369–373 (1998).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Carandini, M. & Heeger, D. J. Summation and division by neurons in primate visual cortex. Science 264, 1333 –1336 (1994).

    Article  CAS  Google Scholar 

  28. Merrill, E. G. & Ainsworth, A. Glass-coated platinum-plated tungsten microelectrodes. Med. Biol. Eng. 10, 662–672 (1972).

    Article  CAS  Google Scholar 

  29. Lund, J. S., Hendrickson, A. E., Ogren, M. P. & Tobin, E. A. Anatomical organization of primate visual cortex area V1. J. Comp. Neurol. 202, 19–45 ( 1981).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Shasta Sabo and Haim Sompolinsky for their comments. Lorraine Smith assisted in the histological reconstruction and during physiology experiments. This work was supported by National Institute of Health grants EY01472 and EY08300 and Sloan Foundation Grant in Theoretical Neuroscience 97-12-3.

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Correspondence to Michael P. Sceniak.

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Sceniak, M., Ringach, D., Hawken, M. et al. Contrast's effect on spatial summation by macaque V1 neurons. Nat Neurosci 2, 733–739 (1999). https://doi.org/10.1038/11197

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