A new no-report paradigm reveals that face cells encode both consciously perceived and suppressed stimuli
Abstract
A powerful paradigm to identify neural correlates of consciousness is binocular rivalry, wherein a constant visual stimulus evokes a varying conscious percept. It has recently been suggested that activity modulations observed during rivalry may represent the act of report rather than the conscious percept itself. Here, we performed single-unit recordings from face patches in macaque inferotemporal (IT) cortex using a no-report paradigm in which the animal's conscious percept was inferred from eye movements. We found that high proportions of IT neurons represented the conscious percept even without active report. Furthermore, on single trials we could decode both the conscious percept and the suppressed stimulus. Together, these findings indicate that (1) IT cortex possesses a true neural correlate of consciousness, and (2) this correlate consists of a population code wherein single cells multiplex representation of the conscious percept and veridical physical stimulus, rather than a subset of cells perfectly reflecting consciousness.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files.
Article and author information
Author details
Funding
Howard Hughes Medical Institute
- Doris Y Tsao
Simons Foundation
- Doris Y Tsao
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 animal procedures in this study complied with local and National Institute of Health guidelines including the US National Institutes of Health Guide for Care and Use of Laboratory Animals. All experiments were performed with the approval of the Caltech Institutional Animal Care and Use Committee (IACUC), under protocol #1574.
Human subjects: The behavioral experiment with human subjects for the human psychophysics experiment complied with a protocol approved by the Caltech Institutional Review Board (IRB 19-0903). Informed consent was obtained from all subjects.
Reviewing Editor
- Ming Meng, South China Normal University, China
Version history
- Received: April 28, 2020
- Accepted: November 9, 2020
- Accepted Manuscript published: November 11, 2020 (version 1)
- Version of Record published: November 19, 2020 (version 2)
Copyright
© 2020, Hesse & Tsao
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
-
- 3,642
- Page views
-
- 555
- Downloads
-
- 14
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
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)
Further reading
-
- Neuroscience
Ultrasonic vocalizations (USVs) fulfill an important role in communication and navigation in many species. Because of their social and affective significance, rodent USVs are increasingly used as a behavioral measure in neurodevelopmental and neurolinguistic research. Reliably attributing USVs to their emitter during close interactions has emerged as a difficult, key challenge. If addressed, all subsequent analyses gain substantial confidence. We present a hybrid ultrasonic tracking system, Hybrid Vocalization Localizer (HyVL), that synergistically integrates a high-resolution acoustic camera with high-quality ultrasonic microphones. HyVL is the first to achieve millimeter precision (~3.4–4.8 mm, 91% assigned) in localizing USVs, ~3× better than other systems, approaching the physical limits (mouse snout ~10 mm). We analyze mouse courtship interactions and demonstrate that males and females vocalize in starkly different relative spatial positions, and that the fraction of female vocalizations has likely been overestimated previously due to imprecise localization. Further, we find that when two male mice interact with one female, one of the males takes a dominant role in the interaction both in terms of the vocalization rate and the location relative to the female. HyVL substantially improves the precision with which social communication between rodents can be studied. It is also affordable, open-source, easy to set up, can be integrated with existing setups, and reduces the required number of experiments and animals.
-
- Neuroscience
How does the human brain combine information across the eyes? It has been known for many years that cortical normalization mechanisms implement ‘ocularity invariance’: equalizing neural responses to spatial patterns presented either monocularly or binocularly. Here, we used a novel combination of electrophysiology, psychophysics, pupillometry, and computational modeling to ask whether this invariance also holds for flickering luminance stimuli with no spatial contrast. We find dramatic violations of ocularity invariance for these stimuli, both in the cortex and also in the subcortical pathways that govern pupil diameter. Specifically, we find substantial binocular facilitation in both pathways with the effect being strongest in the cortex. Near-linear binocular additivity (instead of ocularity invariance) was also found using a perceptual luminance matching task. Ocularity invariance is, therefore, not a ubiquitous feature of visual processing, and the brain appears to repurpose a generic normalization algorithm for different visual functions by adjusting the amount of interocular suppression.