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Thalamocortical NMDA conductances and intracortical inhibition can explain cortical temporal tuning

Nature Neuroscience volume 4, pages 424–430 (2001)Cite this article

Abstract

Cells in cerebral cortex fail to respond to fast-moving stimuli that evoke strong responses in the thalamic nuclei innervating the cortex. The reason for this behavior has remained a mystery. We study an experimentally motivated model of the thalamic input-recipient layer of cat primary visual cortex that accounts for many aspects of cortical orientation tuning. In this circuit, inhibition dominates over excitation, but temporal modulations of excitation and inhibition occur out of phase with one another, allowing excitation to transiently drive cells. We show that this circuit provides a natural explanation of cortical low-pass temporal frequency tuning, provided N-methyl-d-aspartate (NMDA) receptors are present in thalamocortical synapses in proportions measured experimentally. This suggests a new and unanticipated role for NMDA conductances in shaping the temporal response properties of cortical cells, and suggests that common cortical circuit mechanisms underlie both spatial and temporal response tuning.

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Figure 1: Overview of the model and its behavior.
Figure 2: Quantitation of model temporal tuning and main parameter dependence.
Figure 3: Temporal frequency tuning of the model with different levels of NMDA in the feedback excitatory connections.

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Acknowledgements

We thank T. Troyer for discussions and L. Stone for comments on the manuscript. Supported by a Howard Hughes Medical Institute predoctoral fellowship (A.E.K.) and by RO1EY001 from the National Eye Institute (K.D.M.).

Author information

Author notes

  1. Anton E. Krukowski

    Present address: NASA Ames Research Center, Mail Stop 262-2, Moffett Field, California, 94035-1000, USA

Authors and Affiliations

  1. Biophysics Graduate Program, University of California, San Francisco, 94143-0444, California, USA

    Anton E. Krukowski

  2. W. M. Keck Center for Integrative Neuroscience, University of California, San Francisco, 94143-0444, California, USA

    Anton E. Krukowski & Kenneth D. Miller

  3. Department of Physiology, University of California, San Francisco, 94143-0444, California, USA

    Kenneth D. Miller

  4. Department of Otolaryngology, University of California, San Francisco, 94143-0444, California, USA

    Kenneth D. Miller

  5. Sloan-Swartz Center for Theoretical Neurobiology at UCSF, University of California, San Francisco, 94143-0444, California, USA

    Kenneth D. Miller

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  1. Anton E. Krukowski
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Correspondence to Anton E. Krukowski or Kenneth D. Miller.

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Krukowski, A., Miller, K. Thalamocortical NMDA conductances and intracortical inhibition can explain cortical temporal tuning. Nat Neurosci 4, 424–430 (2001). https://doi.org/10.1038/86084

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