Population receptive fields in non-human primates from whole-brain fmri and large-scale neurophysiology in visual cortex

P. Christiaan Klink; Xing Chen; Wim Vanduffel; Pieter R. Roelfsema

doi:10.7554/eLife.67304

Population receptive fields in non-human primates from whole-brain fmri and large-scale neurophysiology in visual cortex

P. Christiaan Klink^*, Xing Chen, Wim Vanduffel, Pieter R. Roelfsema

^*Corresponding author for this work

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

Abstract

Population receptive field (pRF) modeling is a popular fMRI method to map the retinotopic organization of the human brain. While fMRI-based pRF-maps are qualitatively similar to invasively recorded single-cell receptive fields in animals, it remains unclear what neuronal signal they represent. We addressed this question in awake non-human primates comparing whole-brain fMRI and large-scale neurophysiological recordings in areas V1 and V4 of the visual cortex. We examined the fits of several pRF-models based on the fMRI BOLD-signal, multi-unit spiking activity (MUA) and local field potential (LFP) power in different frequency bands. We found that pRFs derived from BOLD-fMRI were most similar to MUA-pRFs in V1 and V4, while pRFs based on LFP gamma power also gave a good approximation. FMRI-based pRFs thus reliably reflect neuronal receptive field properties in the primate brain. In addition to our results in V1 and V4, the whole-brain fMRI measurements revealed retinotopic tuning in many other cortical and subcortical areas with a consistent increase in pRF-size with increasing eccentricity, as well as a retinotopically specific deactivation of default-mode network nodes similar to previous observations in humans.

Original language	English
Article number	e67304
Pages (from-to)	1-35
Number of pages	35
Journal	eLife
Volume	10
DOIs	https://doi.org/10.7554/eLife.67304
Publication status	Published - 3 Nov 2021

Bibliographical note

Funding Information:
785907, “Human Brain Project SGA1 and SGA2”), and the Friends Foundation of the Netherlands Institute

Funding Information:
This work was supported by NWO (Crossover Program 17619 ?INTENSE?; STW-Perspectief P15-42 ?NESTOR?; VENI 451.13.023), the European Union FP7 (ERC 339490 ?Cortic_al_gorithms?), the Human Brain Project (agreements 720270 and 785907, ?Human Brain Project SGA1 and SGA2?), and the Friends Foundation of the Netherlands Institute for Neuroscience.

Funding Information:
We thank Jonathan Williford for his contributions to the fMRI preprocessing pipeline; Pieter Buur, Wietske van der Zwaag, Diederick Stoffers, and the Laboratory of Neuro-and Psychophysiology of KU Leuven for technical assistance in setting up the non-human primate MR infrastructure; Kor Brandsma, Anneke Ditewig, and Lex Beekman for animal care and biotechnical assistance; Feng Wang for help with electrophysiology data collection; Chris van der Togt for help with data management; and Tomas Knapen and Serge Dumoulin for fruitful discussion and comments on an earlier version of the manuscript. This work was supported by NWO (Crossover Program 17619 “INTENSE”; STW-Perspectief P15-42 “NESTOR”; VENI 451.13.023), the European Union FP7 (ERC 339490 “Cortic_al_gorithms”), the Human Brain Project (agreements 720270 and

Publisher Copyright:
© 2021, eLife Sciences Publications Ltd. All rights reserved.

Funding

785907, “Human Brain Project SGA1 and SGA2”), and the Friends Foundation of the Netherlands Institute This work was supported by NWO (Crossover Program 17619 ?INTENSE?; STW-Perspectief P15-42 ?NESTOR?; VENI 451.13.023), the European Union FP7 (ERC 339490 ?Cortic_al_gorithms?), the Human Brain Project (agreements 720270 and 785907, ?Human Brain Project SGA1 and SGA2?), and the Friends Foundation of the Netherlands Institute for Neuroscience. We thank Jonathan Williford for his contributions to the fMRI preprocessing pipeline; Pieter Buur, Wietske van der Zwaag, Diederick Stoffers, and the Laboratory of Neuro-and Psychophysiology of KU Leuven for technical assistance in setting up the non-human primate MR infrastructure; Kor Brandsma, Anneke Ditewig, and Lex Beekman for animal care and biotechnical assistance; Feng Wang for help with electrophysiology data collection; Chris van der Togt for help with data management; and Tomas Knapen and Serge Dumoulin for fruitful discussion and comments on an earlier version of the manuscript. This work was supported by NWO (Crossover Program 17619 “INTENSE”; STW-Perspectief P15-42 “NESTOR”; VENI 451.13.023), the European Union FP7 (ERC 339490 “Cortic_al_gorithms”), the Human Brain Project (agreements 720270 and

Funders	Funder number
Friends Foundation of the Netherlands Institute
Friends Foundation of the Netherlands Institute for Neuroscience
Horizon 2020 Framework Programme	339490, 945539
European Research Council	785907, 720270
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	17619, P15-42, VENI 451.13.023
Seventh Framework Programme

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10.7554/eLife.67304

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title = "Population receptive fields in non-human primates from whole-brain fmri and large-scale neurophysiology in visual cortex",

abstract = "Population receptive field (pRF) modeling is a popular fMRI method to map the retinotopic organization of the human brain. While fMRI-based pRF-maps are qualitatively similar to invasively recorded single-cell receptive fields in animals, it remains unclear what neuronal signal they represent. We addressed this question in awake non-human primates comparing whole-brain fMRI and large-scale neurophysiological recordings in areas V1 and V4 of the visual cortex. We examined the fits of several pRF-models based on the fMRI BOLD-signal, multi-unit spiking activity (MUA) and local field potential (LFP) power in different frequency bands. We found that pRFs derived from BOLD-fMRI were most similar to MUA-pRFs in V1 and V4, while pRFs based on LFP gamma power also gave a good approximation. FMRI-based pRFs thus reliably reflect neuronal receptive field properties in the primate brain. In addition to our results in V1 and V4, the whole-brain fMRI measurements revealed retinotopic tuning in many other cortical and subcortical areas with a consistent increase in pRF-size with increasing eccentricity, as well as a retinotopically specific deactivation of default-mode network nodes similar to previous observations in humans.",

author = "{Christiaan Klink}, P. and Xing Chen and Wim Vanduffel and Roelfsema, {Pieter R.}",

note = "Funding Information: 785907, “Human Brain Project SGA1 and SGA2”), and the Friends Foundation of the Netherlands Institute Funding Information: This work was supported by NWO (Crossover Program 17619 ?INTENSE?; STW-Perspectief P15-42 ?NESTOR?; VENI 451.13.023), the European Union FP7 (ERC 339490 ?Cortic_al_gorithms?), the Human Brain Project (agreements 720270 and 785907, ?Human Brain Project SGA1 and SGA2?), and the Friends Foundation of the Netherlands Institute for Neuroscience. Funding Information: We thank Jonathan Williford for his contributions to the fMRI preprocessing pipeline; Pieter Buur, Wietske van der Zwaag, Diederick Stoffers, and the Laboratory of Neuro-and Psychophysiology of KU Leuven for technical assistance in setting up the non-human primate MR infrastructure; Kor Brandsma, Anneke Ditewig, and Lex Beekman for animal care and biotechnical assistance; Feng Wang for help with electrophysiology data collection; Chris van der Togt for help with data management; and Tomas Knapen and Serge Dumoulin for fruitful discussion and comments on an earlier version of the manuscript. This work was supported by NWO (Crossover Program 17619 “INTENSE”; STW-Perspectief P15-42 “NESTOR”; VENI 451.13.023), the European Union FP7 (ERC 339490 “Cortic_al_gorithms”), the Human Brain Project (agreements 720270 and Publisher Copyright: {\textcopyright} 2021, eLife Sciences Publications Ltd. All rights reserved.",

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N1 - Funding Information: 785907, “Human Brain Project SGA1 and SGA2”), and the Friends Foundation of the Netherlands Institute Funding Information: This work was supported by NWO (Crossover Program 17619 ?INTENSE?; STW-Perspectief P15-42 ?NESTOR?; VENI 451.13.023), the European Union FP7 (ERC 339490 ?Cortic_al_gorithms?), the Human Brain Project (agreements 720270 and 785907, ?Human Brain Project SGA1 and SGA2?), and the Friends Foundation of the Netherlands Institute for Neuroscience. Funding Information: We thank Jonathan Williford for his contributions to the fMRI preprocessing pipeline; Pieter Buur, Wietske van der Zwaag, Diederick Stoffers, and the Laboratory of Neuro-and Psychophysiology of KU Leuven for technical assistance in setting up the non-human primate MR infrastructure; Kor Brandsma, Anneke Ditewig, and Lex Beekman for animal care and biotechnical assistance; Feng Wang for help with electrophysiology data collection; Chris van der Togt for help with data management; and Tomas Knapen and Serge Dumoulin for fruitful discussion and comments on an earlier version of the manuscript. This work was supported by NWO (Crossover Program 17619 “INTENSE”; STW-Perspectief P15-42 “NESTOR”; VENI 451.13.023), the European Union FP7 (ERC 339490 “Cortic_al_gorithms”), the Human Brain Project (agreements 720270 and Publisher Copyright: © 2021, eLife Sciences Publications Ltd. All rights reserved.

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Population receptive fields in non-human primates from whole-brain fmri and large-scale neurophysiology in visual cortex

Abstract

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