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Can homeostatic plasticity in deafferented primary auditory cortex lead to travelling waves of excitation?

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Abstract

Travelling waves of activity in neural circuits have been proposed as a mechanism underlying a variety of neurological disorders, including epileptic seizures, migraine auras and brain injury. The highly influential Wilson-Cowan cortical model describes the dynamics of a network of excitatory and inhibitory neurons. The Wilson-Cowan equations predict travelling waves of activity in rate-based models that have sufficiently reduced levels of lateral inhibition. Travelling waves of excitation may play a role in functional changes in the auditory cortex after hearing loss. We propose that down-regulation of lateral inhibition may be induced in deafferented cortex via homeostatic plasticity mechanisms. We use the Wilson-Cowan equations to construct a spiking model of the primary auditory cortex that includes a novel, mathematically formalized description of homeostatic plasticity. In our model, the homeostatic mechanisms respond to hearing loss by reducing inhibition and increasing excitation, producing conditions under which travelling waves of excitation can emerge. However, our model predicts that the presence of spontaneous activity prevents the development of long-range travelling waves of excitation. Rather, our simulations show short-duration excitatory waves that cancel each other out. We also describe changes in spontaneous firing, synchrony and tuning after simulated hearing loss. With the exception of shifts in characteristic frequency, changes after hearing loss were qualitatively the same as empirical findings. Finally, we discuss possible applications to tinnitus, the perception of sound without an external stimulus.

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Notes

  1. The peak values and variances of the Gaussian functions defined in this subsection are chosen so that a tonal stimulus would only excite a small portion of the pyramidal neurons. See the model response to a 723-Hz pure tone in Fig. 8 for an example.

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Acknowledgements

The authors would like to express their gratitude to the reviewers for important feedback and advice, and to Dr. Jos J. Eggermont for his critical comments on earlier versions of this manuscript.

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Authors and Affiliations

  1. McMaster Integrative Neuroscience Discovery & Study, McMaster University, 1280 Main Street West, Hamilton, ON, Canada, L8S 4K1

    Michael Chrostowski

  2. Department of Electrical and Computer Engineering, McMaster University, 1280 Main Street West, Hamilton, ON, Canada, L8S 4K1

    Le Yang & Ian C. Bruce

  3. Center for Vision Research, York University, 4700 Keele Street, Toronto, ON, Canada, M3J 1P3

    Hugh R. Wilson

  4. Department of Psychology, Neuroscience and Behaviour, McMaster University, 1280 Main Street West, Hamilton, ON, Canada, L8S 4K1

    Suzanna Becker

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  1. Michael Chrostowski
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Correspondence to Michael Chrostowski.

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Action Editor: S. A. Shamma

This research was supported by a New Emerging Teams Grant from the Canadian Institutes of Health Research to S.B. and I.B. and Discovery grants from the Natural Sciences and Engineering Research Council of Canada to S.B and I.B.

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Chrostowski, M., Yang, L., Wilson, H.R. et al. Can homeostatic plasticity in deafferented primary auditory cortex lead to travelling waves of excitation?. J Comput Neurosci 30, 279–299 (2011). https://doi.org/10.1007/s10827-010-0256-1

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