Multisensory task demands temporally extend the causal requirement for visual cortex in perception

Matthijs N. Oude Lohuis; Jean L. Pie; Pietro Marchesi; Jorrit S. Montijn; Christiaan P.J. de Kock; Cyriel M.A. Pennartz; Umberto Olcese

doi:10.1038/s41467-022-30600-4

Multisensory task demands temporally extend the causal requirement for visual cortex in perception

Matthijs N. Oude Lohuis, Jean L. Pie, Pietro Marchesi, Jorrit S. Montijn, Christiaan P.J. de Kock, Cyriel M.A. Pennartz^*, Umberto Olcese

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Primary sensory areas constitute crucial nodes during perceptual decision making. However, it remains unclear to what extent they mainly constitute a feedforward processing step, or rather are continuously involved in a recurrent network together with higher-order areas. We found that the temporal window in which primary visual cortex is required for the detection of identical visual stimuli was extended when task demands were increased via an additional sensory modality that had to be monitored. Late-onset optogenetic inactivation preserved bottom-up, early-onset responses which faithfully encoded stimulus features, and was effective in impairing detection only if it preceded a late, report-related phase of the cortical response. Increasing task demands were marked by longer reaction times and the effect of late optogenetic inactivation scaled with reaction time. Thus, independently of visual stimulus complexity, multisensory task demands determine the temporal requirement for ongoing sensory-related activity in V1, which overlaps with report-related activity.

Original language	English
Article number	2864
Pages (from-to)	1-19
Number of pages	19
Journal	Nature Communications
Volume	13
DOIs	https://doi.org/10.1038/s41467-022-30600-4
Publication status	Published - 23 May 2022

Bibliographical note

Funding Information:
We thank D. Sridharan for providing code for the multi-alternative detection model; C. Rossant, members of the Cortex Lab (UCL) and contributors for Klusta and Phy spike sorting software; Andriana Mantzafou, Klara Gawor, and Alexis Cervàn Canton for assistance in behavioral training. This work was supported by the European Union’s Horizon 2020 Framework Program for Research and Innovation under the Specific Grant Agreement 720270 (Human Brain Project SGA1) to C.M.A.P., Grant Agreement 785907 (Human Brain Project SGA2) and 945539 (Human Brain Project SGA3) to C.M.A.P. and U.O., by the FLAG-ERA JTC 2015 project CANON (co-financed by the Netherlands Organization for Scientific Research—NWO) to U.O., by the FLAG-ERA JTC 2019 project DOMINO (co-financed by NWO) to U.O. and by the Amsterdam Brain and Mind Project to C.M.A.P. and C.P.K.

Funding Information:
We thank D. Sridharan for providing code for the multi-alternative detection model; C. Rossant, members of the Cortex Lab (UCL) and contributors for Klusta and Phy spike sorting software; Andriana Mantzafou, Klara Gawor, and Alexis Cervàn Canton for assistance in behavioral training. This work was supported by the European Union’s Horizon 2020 Framework Program for Research and Innovation under the Specific Grant Agreement 720270 (Human Brain Project SGA1) to C.M.A.P., Grant Agreement 785907 (Human Brain Project SGA2) and 945539 (Human Brain Project SGA3) to C.M.A.P. and U.O., by the FLAG-ERA JTC 2015 project CANON (co-financed by the Netherlands Organization for Scientific Research—NWO) to U.O., by the FLAG-ERA JTC 2019 project DOMINO (co-financed by NWO) to U.O. and by the Amsterdam Brain and Mind Project to C.M.A.P. and C.P.K.

Publisher Copyright:
© 2022, The Author(s).

Funding

We thank D. Sridharan for providing code for the multi-alternative detection model; C. Rossant, members of the Cortex Lab (UCL) and contributors for Klusta and Phy spike sorting software; Andriana Mantzafou, Klara Gawor, and Alexis Cervàn Canton for assistance in behavioral training. This work was supported by the European Union’s Horizon 2020 Framework Program for Research and Innovation under the Specific Grant Agreement 720270 (Human Brain Project SGA1) to C.M.A.P., Grant Agreement 785907 (Human Brain Project SGA2) and 945539 (Human Brain Project SGA3) to C.M.A.P. and U.O., by the FLAG-ERA JTC 2015 project CANON (co-financed by the Netherlands Organization for Scientific Research—NWO) to U.O., by the FLAG-ERA JTC 2019 project DOMINO (co-financed by NWO) to U.O. and by the Amsterdam Brain and Mind Project to C.M.A.P. and C.P.K. We thank D. Sridharan for providing code for the multi-alternative detection model; C. Rossant, members of the Cortex Lab (UCL) and contributors for Klusta and Phy spike sorting software; Andriana Mantzafou, Klara Gawor, and Alexis Cervàn Canton for assistance in behavioral training. This work was supported by the European Union’s Horizon 2020 Framework Program for Research and Innovation under the Specific Grant Agreement 720270 (Human Brain Project SGA1) to C.M.A.P., Grant Agreement 785907 (Human Brain Project SGA2) and 945539 (Human Brain Project SGA3) to C.M.A.P. and U.O., by the FLAG-ERA JTC 2015 project CANON (co-financed by the Netherlands Organization for Scientific Research—NWO) to U.O., by the FLAG-ERA JTC 2019 project DOMINO (co-financed by NWO) to U.O. and by the Amsterdam Brain and Mind Project to C.M.A.P. and C.P.K.

Funders	Funder number
Alexis Cervàn Canton
Cortex Lab
European Union’s Horizon 2020 Framework Program for Research and Innovation
Horizon 2020 Framework Programme	785907, 720270, 945539
University College London
Nederlandse Organisatie voor Wetenschappelijk Onderzoek

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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title = "Multisensory task demands temporally extend the causal requirement for visual cortex in perception",

abstract = "Primary sensory areas constitute crucial nodes during perceptual decision making. However, it remains unclear to what extent they mainly constitute a feedforward processing step, or rather are continuously involved in a recurrent network together with higher-order areas. We found that the temporal window in which primary visual cortex is required for the detection of identical visual stimuli was extended when task demands were increased via an additional sensory modality that had to be monitored. Late-onset optogenetic inactivation preserved bottom-up, early-onset responses which faithfully encoded stimulus features, and was effective in impairing detection only if it preceded a late, report-related phase of the cortical response. Increasing task demands were marked by longer reaction times and the effect of late optogenetic inactivation scaled with reaction time. Thus, independently of visual stimulus complexity, multisensory task demands determine the temporal requirement for ongoing sensory-related activity in V1, which overlaps with report-related activity.",

author = "{Oude Lohuis}, {Matthijs N.} and Pie, {Jean L.} and Pietro Marchesi and Montijn, {Jorrit S.} and {de Kock}, {Christiaan P.J.} and Pennartz, {Cyriel M.A.} and Umberto Olcese",

note = "Funding Information: We thank D. Sridharan for providing code for the multi-alternative detection model; C. Rossant, members of the Cortex Lab (UCL) and contributors for Klusta and Phy spike sorting software; Andriana Mantzafou, Klara Gawor, and Alexis Cerv{\`a}n Canton for assistance in behavioral training. This work was supported by the European Union{\textquoteright}s Horizon 2020 Framework Program for Research and Innovation under the Specific Grant Agreement 720270 (Human Brain Project SGA1) to C.M.A.P., Grant Agreement 785907 (Human Brain Project SGA2) and 945539 (Human Brain Project SGA3) to C.M.A.P. and U.O., by the FLAG-ERA JTC 2015 project CANON (co-financed by the Netherlands Organization for Scientific Research—NWO) to U.O., by the FLAG-ERA JTC 2019 project DOMINO (co-financed by NWO) to U.O. and by the Amsterdam Brain and Mind Project to C.M.A.P. and C.P.K. Funding Information: We thank D. Sridharan for providing code for the multi-alternative detection model; C. Rossant, members of the Cortex Lab (UCL) and contributors for Klusta and Phy spike sorting software; Andriana Mantzafou, Klara Gawor, and Alexis Cerv{\`a}n Canton for assistance in behavioral training. This work was supported by the European Union{\textquoteright}s Horizon 2020 Framework Program for Research and Innovation under the Specific Grant Agreement 720270 (Human Brain Project SGA1) to C.M.A.P., Grant Agreement 785907 (Human Brain Project SGA2) and 945539 (Human Brain Project SGA3) to C.M.A.P. and U.O., by the FLAG-ERA JTC 2015 project CANON (co-financed by the Netherlands Organization for Scientific Research—NWO) to U.O., by the FLAG-ERA JTC 2019 project DOMINO (co-financed by NWO) to U.O. and by the Amsterdam Brain and Mind Project to C.M.A.P. and C.P.K. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

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doi = "10.1038/s41467-022-30600-4",

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AU - Oude Lohuis, Matthijs N.

AU - Pie, Jean L.

AU - Marchesi, Pietro

AU - Montijn, Jorrit S.

AU - de Kock, Christiaan P.J.

AU - Pennartz, Cyriel M.A.

AU - Olcese, Umberto

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Multisensory task demands temporally extend the causal requirement for visual cortex in perception

Abstract

Bibliographical note

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