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Firing-rate based network modeling of the dLGN circuit: Effects of cortical feedback on spatiotemporal response properties of relay cells

Author

Listed:
  • Milad Hobbi Mobarhan
  • Geir Halnes
  • Pablo Martínez-Cañada
  • Torkel Hafting
  • Marianne Fyhn
  • Gaute T Einevoll

Abstract

Visually evoked signals in the retina pass through the dorsal geniculate nucleus (dLGN) on the way to the visual cortex. This is however not a simple feedforward flow of information: there is a significant feedback from cortical cells back to both relay cells and interneurons in the dLGN. Despite four decades of experimental and theoretical studies, the functional role of this feedback is still debated. Here we use a firing-rate model, the extended difference-of-Gaussians (eDOG) model, to explore cortical feedback effects on visual responses of dLGN relay cells. For this model the responses are found by direct evaluation of two- or three-dimensional integrals allowing for fast and comprehensive studies of putative effects of different candidate organizations of the cortical feedback. Our analysis identifies a special mixed configuration of excitatory and inhibitory cortical feedback which seems to best account for available experimental data. This configuration consists of (i) a slow (long-delay) and spatially widespread inhibitory feedback, combined with (ii) a fast (short-delayed) and spatially narrow excitatory feedback, where (iii) the excitatory/inhibitory ON-ON connections are accompanied respectively by inhibitory/excitatory OFF-ON connections, i.e. following a phase-reversed arrangement. The recent development of optogenetic and pharmacogenetic methods has provided new tools for more precise manipulation and investigation of the thalamocortical circuit, in particular for mice. Such data will expectedly allow the eDOG model to be better constrained by data from specific animal model systems than has been possible until now for cat. We have therefore made the Python tool pyLGN which allows for easy adaptation of the eDOG model to new situations.Author summary: On route from the retina to primary visual cortex, visually evoked signals have to pass through the dorsal lateral geniculate nucleus (dLGN). However, this is not an exclusive feedforward flow of information as feedback exists from neurons in the cortex back to both relay cells and interneurons in the dLGN. The functional role of this feedback remains mostly unresolved. Here, we use a firing-rate model, the extended difference-of-Gaussians (eDOG) model, to explore cortical feedback effects on visual responses of dLGN relay cells. Our analysis indicates that a particular mix of excitatory and inhibitory cortical feedback agrees best with available experimental observations. In this configuration ON-center relay cells receive both excitatory and (indirect) inhibitory feedback from ON-center cortical cells (ON-ON feedback) where the excitatory feedback is fast and spatially narrow while the inhibitory feedback is slow and spatially widespread. In addition to the ON-ON feedback, the connections are accompanied by OFF-ON connections following a so-called phase-reversed (push-pull) arrangement. To facilitate further applications of the model, we have made the Python tool pyLGN which allows for easy modification and evaluation of the a priori quite general eDOG model to new situations.

Suggested Citation

  • Milad Hobbi Mobarhan & Geir Halnes & Pablo Martínez-Cañada & Torkel Hafting & Marianne Fyhn & Gaute T Einevoll, 2018. "Firing-rate based network modeling of the dLGN circuit: Effects of cortical feedback on spatiotemporal response properties of relay cells," PLOS Computational Biology, Public Library of Science, vol. 14(5), pages 1-38, May.
  • Handle: RePEc:plo:pcbi00:1006156
    DOI: 10.1371/journal.pcbi.1006156
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    References listed on IDEAS

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    1. Shawn R. Olsen & Dante S. Bortone & Hillel Adesnik & Massimo Scanziani, 2012. "Gain control by layer six in cortical circuits of vision," Nature, Nature, vol. 483(7387), pages 47-52, March.
    2. Gaute T Einevoll & Paulius Jurkus & Paul Heggelund, 2011. "Coarse-to-Fine Changes of Receptive Fields in Lateral Geniculate Nucleus Have a Transient and a Sustained Component That Depend on Distinct Mechanisms," PLOS ONE, Public Library of Science, vol. 6(9), pages 1-19, September.
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