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

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

44 Downloads (Pure)

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
Number of pages15
JournalCurrent Biology
Volume29
Issue number24
Early online date27 Nov 2019
DOIs
Publication statusPublished - 16 Dec 2019

Funding

We thank Hadi Saiepour, Mehran Ahmadlou, and Emma Ruimschotel for assistance. We gratefully acknowledge Vivek Jayaraman, Rex Kerr, Douglas Kim, Loren Looger, and Karel Svoboda from the GENIE Project, Janelia Farm Research Campus, Howard Hughes Medical Institute for the GCaMP6 vectors and Josh Huang and his colleagues from the NIH Neuroscience Blueprint Cre Driver Network for the Sst-IRES-Cre mice. J.V. was funded by a Marie Curie IEF grant. J.V., M.X.C., and J.A.H. were funded by NWO VIDI grant 864.10.010 . P.R.R. was funded by ERC advanced grant 39490 “Cortic_al_gorithms,” NWO-ALW grant 823.02.010 , the Human Brain Project (grant agreement no. 720270 - HBP SGA1 ), and the Erasmus Mundus Neurotime Program. C.N.L. received funding from the European Union’s Horizon 2020 Research and Innovation Programme under grant agreement no. 720270 (HBP SGA1).

FundersFunder number
Hadi Saiepour
Mehran Ahmadlou
Vivek Jayaraman, Rex Kerr
National Institutes of Health
Horizon 2020 Framework Programme
European Research Council39490
Nederlandse Organisatie voor Wetenschappelijk Onderzoek720270, 864.10.010, 823.02.010
Horizon 2020

    Keywords

    • feedback
    • inhibition
    • mouse
    • primary visual cortex
    • surround suppression

    Fingerprint

    Dive into the research topics of 'Activity in Lateral Visual Areas Contributes to Surround Suppression in Awake Mouse V1'. Together they form a unique fingerprint.

    Cite this