TY - JOUR
T1 - Activity in Lateral Visual Areas Contributes to Surround Suppression in Awake Mouse V1
AU - Vangeneugden, Joris
AU - van Beest, Enny H.
AU - Cohen, Michael X.
AU - Lorteije, Jeannette A. M.
AU - Mukherjee, Sreedeep
AU - Kirchberger, Lisa
AU - Montijn, Jorrit S.
AU - Thamizharasu, Premnath
AU - Camillo, Daniela
AU - Levelt, Christiaan N.
AU - Roelfsema, Pieter R.
AU - Self, Matthew W.
AU - Heimel, J. Alexander
N1 - Funding Information:
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). Conceptualization, J.V. P.R.R. M.W.S. and J.A.H.; Methodology, J.V. M.W.S. and J.A.H.; Software, M.X.C. M.W.S. and J.A.H.; Investigation, J.V. E.H.v.B. M.X.C. J.A.M.L. S.M. L.K. J.S.M. P.T. D.C. M.W.S. and J.A.H.; Resources, C.N.L. P.R.R. and J.A.H.; Writing – Original Draft, M.W.S. and J.A.H.; Writing – Review & Editing, J.V. E.H.v.B. M.X.C. J.A.M.L. C.N.L. P.R.R. M.W.S. and J.A.H.; Supervision, M.W.S. and J.A.H.; Funding Acquisition, C.N.L. P.R.R. and J.A.H. The authors declare no competing interests.
Funding Information:
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).
Publisher Copyright:
© 2019 Elsevier Ltd
PY - 2019/12/16
Y1 - 2019/12/16
N2 - 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.
AB - 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.
KW - CLASSICAL RECEPTIVE-FIELD
KW - FEEDBACK CONNECTIONS
KW - CORTEX
KW - NEURONS
KW - FEEDFORWARD
KW - INHIBITION
KW - CIRCUIT
KW - ORGANIZATION
KW - Classical receptive-field
KW - Organization
KW - Neurons
KW - Cortex
KW - Circuit
KW - Inhibition
KW - Feedforward
KW - Feedback connections
U2 - 10.1016/j.cub.2019.10.037
DO - 10.1016/j.cub.2019.10.037
M3 - Article
C2 - 31786063
SN - 0960-9822
VL - 29
SP - 4268-4275.e7
JO - Current Biology
JF - Current Biology
IS - 24
ER -