Neural dynamics at successive stages of the ventral visual stream are consistent with hierarchical error signals

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Abstract

Ventral visual stream neural responses are dynamic, even for static image presentations. However, dynamical neural models of visual cortex are lacking as most progress has been made modeling static, time-averaged responses. Here, we studied population neural dynamics during face detection across three cortical processing stages. Remarkably, ~30 milliseconds after the initially evoked response, we found that neurons in intermediate level areas decreased their responses to typical configurations of their preferred face parts relative to their response for atypical configurations even while neurons in higher areas achieved and maintained a preference for typical configurations. These hierarchical neural dynamics were inconsistent with standard feedforward circuits. Rather, recurrent models computing prediction errors between stages captured the observed temporal signatures. This model of neural dynamics, which simply augments the standard feedforward model of online vision, suggests that neural responses to static images may encode top-down prediction errors in addition to bottom-up feature estimates.

Data availability

All data generated or analyzed during this study are included in the supporting files for the manuscript. Source data files have been provided for Figures 1-5, and code for computational models in Figures 5 & 6 is provided.

Article and author information

Author details

Elias B Issa

McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States

For correspondence
elias.issa@columbia.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5387-7207
Charles F Cadieu

McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States

Competing interests
The authors declare that no competing interests exist.
Jim DiCarlo

McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States

Competing interests
The authors declare that no competing interests exist.

Funding

National Institutes of Health (R01-EY014970)

Jim DiCarlo

National Institutes of Health (K99-EY022671)

Elias B Issa

National Institutes of Health (F32-EY019609)

Elias B Issa

National Institutes of Health (F32-EY022845)

Charles F Cadieu

Office of Naval Research (MURI-114407)

Jim DiCarlo

McGovern Institute for Brain Research

Jim DiCarlo

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

Ethics

Animal experimentation: All procedures were performed in compliance with National Institutes of Health guidelines and the standards of the MIT Committee on Animal Care (IACUC protocol #0111-003-14) and the American Physiological Society.

Copyright

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.