V1 neurons are tuned to perceptual borders in natural scenes

Paolo Papale, Wietske Zuiderbaan, Rob R.M. Teeuwen, Amparo Gilhuis, Matthew W. Self, Pieter R. Roelfsema, Serge O. Dumoulin

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

The visual system needs to identify perceptually relevant borders to segment complex natural scenes. The primary visual cortex (V1) is thought to extract local borders, and higher visual areas are thought to identify the perceptually relevant borders between objects and the background. To test this conjecture, we used natural images that had been annotated by human observers who marked the perceptually relevant borders. We assessed the effect of perceptual relevance on V1 responses using human neuroimaging, macaque electrophysiology, and computational modeling. We report that perceptually relevant borders elicit stronger responses in the early visual cortex than irrelevant ones, even if simple features, such as contrast and the energy of oriented filters, are matched. Moreover, V1 neurons discriminate perceptually relevant borders surprisingly fast, during the early feedforward-driven activity at a latency of ~50 ms, indicating that they are tuned to the features that characterize them. We also revealed a delayed, contextual effect that enhances the V1 responses that are elicited by perceptually relevant borders at a longer latency. Our results reveal multiple mechanisms that allow V1 neurons to infer the layout of objects in natural images.

Original languageEnglish
Article numbere2221623121
Pages (from-to)1-10
Number of pages10
JournalProceedings of the National Academy of Sciences of the United States of America
Volume121
Issue number46
Early online date4 Nov 2024
DOIs
Publication statusPublished - 12 Nov 2024

Funding

ACKNOWLEDGMENTS. We thank Kor Brandsma and Anneke Ditewig for biotechnical support. The work was supported by the European Union\u2019s Horizon 2020 and FP7 Research and Innovation Program (Framework Partnership Agreement No. 650003 [Human Brain Project Framework Partnership Agreement], European Research Council advanced grant 101052963 \u201CNUMEROUS\u201D and grant agreement 899287 \u201CNeuraViper\u201D),\u201CDBI2,\u201D a Gravitation program of the Dutch Ministry of Science, Education and Culture) and the Netherlands Organization for Scientific Research (NWO) Crossover Program 17619 \u201CINTENSE\u201D to P.R.R.,the European Union\u2019s Erasmus+ program (2018-1-IT02-KA103-047276/10), the NWO Open-Competition Domain Science\u2013XS (OCENW.XS22.2.097) and the NWO Veni (VI.Veni.222.217) to P.P.and the NWO Vidi (452.08.008) and Vici (016.vici.185.050) to S.O.D. We thank Kor Brandsma and Anneke Ditewig for biotechnical support. The work was supported by the European Union's Horizon 2020 and FP7 Research and Innovation Program (Framework Partnership Agreement No. 650003 [Human Brain Project Framework Partnership Agreement], European Research Council advanced grant 101052963 \"NUMEROUS\" and grant agreement 899287 \"NeuraViper\"), \"DBI2, \" a Gravitation program of the Dutch Ministry of Science, Education and Culture) and the Netherlands Organization for Scientific Research (NWO) Crossover Program 17619 \"INTENSE\" to P.R.R., the European Union's Erasmus+ program (2018-1-IT02-KA103-047276/10), the NWO Open-Competition Domain Science-XS (OCENW.XS22.2.097) and the NWO Veni (VI.Veni.222.217) to P.P. and the NWO Vidi (452.08.008) and Vici (016.vici.185.050) to S.O.D.

FundersFunder number
NWO Open-Competition Domain Science
Horizon 2020 Framework Programme
European Commission
Dutch Ministry of Science, Education and Culture
European Research Council899287, 101052963
European Research Council
Nederlandse Organisatie voor Wetenschappelijk OnderzoekOCENW.XS22.2.097, 2018-1-IT02-KA103-047276/10, 17619, 452.08.008, VI.Veni.222.217
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
FP7 Research and Innovation Program650003

    Keywords

    • fmri
    • natural vision
    • neurophysiology
    • nonhuman primates
    • V1

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