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

  1. Peter Christiaan Klink  Is a corresponding author
  2. Xing Chen
  3. Vim Vanduffel
  4. Pieter Roelfsema
  1. Netherlands Institute for Neuroscience, Netherlands
  2. KU Leuven Medical School, Belgium

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.

Data availability

- All data and code are available on GIN: https://doi.org/10.12751/g-node.p8ypgv- Unthresholded fMRI model fitting results are available on Neurovault: https://identifiers.org/neurovault.collection:8082

Article and author information

Author details

  1. Peter Christiaan Klink

    Vision and Cognition, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    For correspondence
    c.klink@nin.knaw.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6784-7842
  2. Xing Chen

    Vision and Cognition, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3589-1750
  3. Vim Vanduffel

    KU Leuven Medical School, Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  4. Pieter Roelfsema

    Vision and Cognition, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1625-0034

Funding

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (VENI 451.13.023)

  • Peter Christiaan Klink

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (STW-Perspectief P15-42 NESTOR"")

  • Xing Chen
  • Pieter Roelfsema

FP7 Ideas: European Research Council (ERC 339490 Cortic_al_gorithms"")

  • Pieter Roelfsema

Human Brain Project ((agreements 720270 and 785907,Human Brain Project SGA1 and SGA2"")

  • Vim Vanduffel
  • Pieter Roelfsema

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (Crossover Program 17619 INTENSE"")

  • Peter Christiaan Klink
  • Pieter Roelfsema

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Animal care and experimental procedures were in accordance with the ILAR's Guide for the Care and Use of Laboratory Animals, the European legislation (Directive 2010/63/EU) and approved by the institutional animal care and use committee of the Royal Netherlands Academy of Arts and Sciences and the Central Authority for Scientific Procedures on Animals (CCD) in the Netherlands (License numbers AVD8010020173789 and AVD8010020171046).

Copyright

© 2021, Klink et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,628
    views
  • 362
    downloads
  • 34
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Peter Christiaan Klink
  2. Xing Chen
  3. Vim Vanduffel
  4. Pieter Roelfsema
(2021)
Population receptive fields in non-human primates from whole-brain fMRI and large-scale neurophysiology in visual cortex in visual cortex
eLife 10:e67304.
https://doi.org/10.7554/eLife.67304

Share this article

https://doi.org/10.7554/eLife.67304

Further reading

    1. Developmental Biology
    2. Neuroscience
    Agnik Dasgupta, Caleb C Reagor ... AJ Hudspeth
    Research Article

    In a developing nervous system, axonal arbors often undergo complex rearrangements before neural circuits attain their final innervation topology. In the lateral line sensory system of the zebrafish, developing sensory axons reorganize their terminal arborization patterns to establish precise neural microcircuits around the mechanosensory hair cells. However, a quantitative understanding of the changes in the sensory arbor morphology and the regulators behind the microcircuit assembly remain enigmatic. Here, we report that Semaphorin7A (Sema7A) acts as an important mediator of these processes. Utilizing a semi-automated three-dimensional neurite tracing methodology and computational techniques, we have identified and quantitatively analyzed distinct topological features that shape the network in wild-type and Sema7A loss-of-function mutants. In contrast to those of wild-type animals, the sensory axons in Sema7A mutants display aberrant arborizations with disorganized network topology and diminished contacts to hair cells. Moreover, ectopic expression of a secreted form of Sema7A by non-hair cells induces chemotropic guidance of sensory axons. Our findings propose that Sema7A likely functions both as a juxtracrine and as a secreted cue to pattern neural circuitry during sensory organ development.

    1. Neuroscience
    Eun Joo Kim, Mi-Seon Kong ... Jeansok John Kim
    Research Article

    Pavlovian fear conditioning research suggests that the interaction between the dorsal periaqueductal gray (dPAG) and basolateral amygdala (BLA) acts as a prediction error mechanism in the formation of associative fear memories. However, their roles in responding to naturalistic predatory threats, characterized by less explicit cues and the absence of reiterative trial-and-error learning events, remain unexplored. In this study, we conducted single-unit recordings in rats during an ‘approach food-avoid predator’ task, focusing on the responsiveness of dPAG and BLA neurons to a rapidly approaching robot predator. Optogenetic stimulation of the dPAG triggered fleeing behaviors and increased BLA activity in naive rats. Notably, BLA neurons activated by dPAG stimulation displayed immediate responses to the robot, demonstrating heightened synchronous activity compared to BLA neurons that did not respond to dPAG stimulation. Additionally, the use of anterograde and retrograde tracer injections into the dPAG and BLA, respectively, coupled with c-Fos activation in response to predatory threats, indicates that the midline thalamus may play an intermediary role in innate antipredatory-defensive functioning.