Population receptive fields in nonhuman primates from whole-brain fMRI and large-scale neurophysiology in visual cortex.

P Christiaan Klink,Wim Vanduffel,Xing Chen,Pieter R Roelfsema

doi:10.7554/elife.67304

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 nonhuman 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 blood-oxygen-level-dependent (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.

Highlights

55 The concept of a receptive field (RF) is crucial for our understanding of the mechanisms underlying perception, cognition, and action
In our analysis of population receptive field’ (pRF) based on blood-oxygen-level-dependent signal (BOLD), multi-unit spiking activity (MUA) and local field potential (LFP), we explored several pRF models, allowing us to investigate the potential presence of nonlinear spatial summation and negative pRFs
Our comparison of fMRI with large-scale neurophysiological recordings in visual cortex revealed that pRFs derived from the BOLD signal resemble MUA RFs

Summary

Introduction

55 The concept of a receptive field (RF) is crucial for our understanding of the mechanisms underlying perception, cognition, and action. The method is popular and has been used to map a range of visual and cognitive functions (Binda et al, 2018; Ekman et al, 2020; Harvey et al, 2020, 2015; He et al, 2019; Hughes et al, 2019; Mo et al., 2017; Poltoratski et al, 2019; Poltoratski and Tong, 2020; Puckett et al, 2020; Shao et al, 2013; Shen et al., 2020; Silson et al, 2018; Stoll et al, 2020; Thomas et al, 2015; Welbourne et al, 2018; Zuiderbaan et al, 2017), dysfunctions (Ahmadi et al, 2020; Alvarez et al, 2020; Best et al, 2019; Dumoulin and Knapen, 2018; Green et al, 2019; Schwarzkopf et al, 2014), mechanisms of brain development (Dekker et al, 2019), cortical evolution (Keliris et al, 2019; Kolster et al, 2014; Zhu and Vanduffel, 2019), and information transfer across different brain areas (Haak et al, 2013)

Results

Discussion

Conclusion