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Neural field model to reconcile structure with function in primary visual cortex

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  • James Rankin
  • Frédéric Chavane

Abstract

Voltage-sensitive dye imaging experiments in primary visual cortex (V1) have shown that local, oriented visual stimuli elicit stable orientation-selective activation within the stimulus retinotopic footprint. The cortical activation dynamically extends far beyond the retinotopic footprint, but the peripheral spread stays non-selective—a surprising finding given a number of anatomo-functional studies showing the orientation specificity of long-range connections. Here we use a computational model to investigate this apparent discrepancy by studying the expected population response using known published anatomical constraints. The dynamics of input-driven localized states were simulated in a planar neural field model with multiple sub-populations encoding orientation. The realistic connectivity profile has parameters controlling the clustering of long-range connections and their orientation bias. We found substantial overlap between the anatomically relevant parameter range and a steep decay in orientation selective activation that is consistent with the imaging experiments. In this way our study reconciles the reported orientation bias of long-range connections with the functional expression of orientation selective neural activity. Our results demonstrate this sharp decay is contingent on three factors, that long-range connections are sufficiently diffuse, that the orientation bias of these connections is in an intermediate range (consistent with anatomy) and that excitation is sufficiently balanced by inhibition. Conversely, our modelling results predict that, for reduced inhibition strength, spurious orientation selective activation could be generated through long-range lateral connections. Furthermore, if the orientation bias of lateral connections is very strong, or if inhibition is particularly weak, the network operates close to an instability leading to unbounded cortical activation.Author Summary: Optical imaging techniques can reveal the dynamical patterns of cortical activation that encode low-level visual features like position and orientation, which are shaped by both feed-forward projections, recurrent and long-range intra-cortical connections. Anatomical studies have characterized intra-cortical connections, however, it is non-trivial to predict from this data how evoked activity might spread across cortex. Indeed, there remains an apparent conflict between the reported orientation bias of cortical connections, and imaging studies on the propagation of cortical activity. Our study reconciles structure (anatomy) with function (evoked activity) using a dynamic neural field model that predicts the dynamics of cortical activation in a setting both inspired by and parametrically matched to the available anatomical data.

Suggested Citation

  • James Rankin & Frédéric Chavane, 2017. "Neural field model to reconcile structure with function in primary visual cortex," PLOS Computational Biology, Public Library of Science, vol. 13(10), pages 1-30, October.
  • Handle: RePEc:plo:pcbi00:1005821
    DOI: 10.1371/journal.pcbi.1005821
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    References listed on IDEAS

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    1. Lyle Muller & Alexandre Reynaud & Frédéric Chavane & Alain Destexhe, 2014. "The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave," Nature Communications, Nature, vol. 5(1), pages 1-14, May.
    2. Manuel Schottdorf & Stephen J Eglen & Fred Wolf & Wolfgang Keil, 2014. "Can Retinal Ganglion Cell Dipoles Seed Iso-Orientation Domains in the Visual Cortex?," PLOS ONE, Public Library of Science, vol. 9(1), pages 1-18, January.
    3. Kevan A. C. Martin & Stephan Roth & Elisha S. Rusch, 2014. "Superficial layer pyramidal cells communicate heterogeneously between multiple functional domains of cat primary visual cortex," Nature Communications, Nature, vol. 5(1), pages 1-13, December.
    4. Valentin Markounikau & Christian Igel & Amiram Grinvald & Dirk Jancke, 2010. "A Dynamic Neural Field Model of Mesoscopic Cortical Activity Captured with Voltage-Sensitive Dye Imaging," PLOS Computational Biology, Public Library of Science, vol. 6(9), pages 1-14, September.
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