The cortico-thalamic loop attunes competitive lateral interactions across retinotopic and orientation preference maps

Abstract

In the early visual system, corticothalamic feedback projections greatly outnumber thalamocortical feedforward projections. Extensive experimental and modeling work has been devoted to the functional impact of the feedforward pathway, but the role of its denser feedback counterpart remains elusive. Here, we propose a novel unifying framework where thalamic recurrent interactions and corticothalamic feedback act in a closed-loop fashion to attune multiple stimulus representations. At each position of the visual field, the loop puts into competition local representations of the stimulus in thalamus and cortex through direct excitation of narrow topologically-aligned portions of the thalamus, accompanied with peri-geniculate nucleus mediated broad inhibition suppressing the topological surround. We built a detailed conductance-based spiking model incorporating retinal input, lateral geniculate nucleus, peri-geniculate nucleus, primary visual cortex, and all the relevant intra-areal and feedback pathways. For the first time we perform comparative analyses between model configurations with completely or locally inactivated cortico-thalamic feedback, as in the experimental preparations. The model mechanistically explains (i) the existence of intra-thalamic surround suppression, (ii) the sensitivity of thalamic neurons to orientation tuning, (iii) the cortex-dependent center-surround opponency in thalamic cells, (iv) the cortical increase of size and orientation selectivity, (v) the cortically enhanced competition between cross-oriented domains within the hypercolumn, and (vi) the selective suppression of cortical functional connectivity. Our results integrate decades of experimental and theoretical research, supporting the hypothesis that cortico-thalamic loop exerts competitive influence between neighboring regions in the thalamus and cortex, complementing the lateral intra-V1 interactions in center-surround contextual modulation.