Activity in Lateral Visual Areas Contributes to Surround Suppression in Awake Mouse V1

Joris Vangeneugden, Enny H van Beest, Michael X Cohen, Jeannette A M Lorteije, Sreedeep Mukherjee, Lisa Kirchberger, Jorrit S Montijn, Premnath Thamizharasu, Daniela Camillo, Christiaan N Levelt, Pieter R Roelfsema, Matthew W Self, J Alexander Heimel

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Abstract

Neuronal response to sensory stimuli depends on the context. The response in primary visual cortex (V1), for instance, is reduced when a stimulus is surrounded by a similar stimulus [1-3]. The source of this surround suppression is partially known. In mouse, local horizontal integration by somatostatin-expressing interneurons contributes to surround suppression [4]. In primates, however, surround suppression arises too quickly to come from local horizontal integration alone, and myelinated axons from higher visual areas, where cells have larger receptive fields, are thought to provide additional surround suppression [5, 6]. Silencing higher visual areas indeed decreased surround suppression in the awake primate by increasing responses to large stimuli [7, 8], although not under anesthesia [9, 10]. In smaller mammals, like mice, fast surround suppression could be possible without feedback. Recent studies revealed a small reduction in V1 responses when silencing higher areas [11, 12] but have not investigated surround suppression. To determine whether higher visual areas contribute to V1 surround suppression, even when this is not necessary for fast processing, we inhibited the areas lateral to V1, particularly the lateromedial area (LM), a possible homolog of primate V2 [13], while recording in V1 of awake and anesthetized mice. We found that part of the surround suppression depends on activity from lateral visual areas in the awake, but not anesthetized, mouse. Inhibiting the lateral visual areas specifically increased responses in V1 to large stimuli. We present a model explaining how excitatory feedback to V1 can have these suppressive effects for large stimuli.

Original languageEnglish
Pages (from-to)4268-4275.e7
JournalCurrent Biology
Volume29
Issue number24
DOIs
Publication statusPublished - 16 Dec 2019

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    Vangeneugden, J., van Beest, E. H., Cohen, M. X., Lorteije, J. A. M., Mukherjee, S., Kirchberger, L., Montijn, J. S., Thamizharasu, P., Camillo, D., Levelt, C. N., Roelfsema, P. R., Self, M. W., & Heimel, J. A. (2019). Activity in Lateral Visual Areas Contributes to Surround Suppression in Awake Mouse V1. Current Biology, 29(24), 4268-4275.e7. https://doi.org/10.1016/j.cub.2019.10.037