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Research Article

Decoding of the other’s focus of attention by a temporal cortex module

View ORCID ProfileHamidreza Ramezanpour and Peter Thier
PNAS February 4, 2020 117 (5) 2663-2670; first published January 21, 2020 https://doi.org/10.1073/pnas.1911269117
Hamidreza Ramezanpour
aDepartment of Cognitive Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, 72076 Tübingen, Germany;bGraduate School of Neural and Behavioural Sciences, University of Tübingen, 72074 Tübingen, Germany;cInternational Max Planck Research School for Cognitive and Systems Neuroscience, University of Tübingen, 72074 Tübingen, Germany;
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  • ORCID record for Hamidreza Ramezanpour
  • For correspondence: hamidreza.ramezanpour@uni-tuebingen.de thier@uni-tuebingen.de
Peter Thier
aDepartment of Cognitive Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, 72076 Tübingen, Germany;dWerner Reichardt Centre for Integrative Neuroscience, University of Tübingen, 72076 Tübingen, Germany
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  • For correspondence: hamidreza.ramezanpour@uni-tuebingen.de thier@uni-tuebingen.de
  1. Edited by Leslie G. Ungerleider, National Institute of Mental Health, Bethesda, MD, and approved December 24, 2019 (received for review July 3, 2019)

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Significance

We follow the other’s gaze to objects of interest to the other and share attention to the object, a key step toward a theory of (the other’s) mind. Monkeys also follow gaze and establish joint attention. Although monkeys depend more on head gaze (i.e., the orientation of the other’s face) than humans, monkey gaze following exhibits many parallels to human gaze following, rendering monkeys the perfect model for studies of its neural underpinnings. Here we report the identification of a gaze following hub in the monkey superior temporal characterized by neurons that link information on the other’s gaze with distinct targets. Importantly, this link is modifiable by contextual information, allowing the executive control of gaze following.

Abstract

Faces attract the observer’s attention toward objects and locations of interest for the other, thereby allowing the two agents to establish joint attention. Previous work has delineated a network of cortical “patches” in the macaque cortex, processing faces, eventually also extracting information on the other’s gaze direction. Yet, the neural mechanism that links information on gaze direction, guiding the observer’s attention to the relevant object, has remained elusive. Here we present electrophysiological evidence for the existence of a distinct “gaze-following patch” (GFP) with neurons that establish this linkage in a highly flexible manner. The other’s gaze and the object, singled out by the gaze, are linked only if this linkage is pertinent within the prevailing social context. The properties of these neurons establish the GFP as a key switch in controlling social interactions based on the other’s gaze.

  • gaze-following patch
  • social interactions
  • joint attention
  • superior temporal sulcus
  • spatial attention

Footnotes

  • ↵1To whom correspondence may be addressed. Email: hamidreza.ramezanpour{at}uni-tuebingen.de or thier{at}uni-tuebingen.de.
  • Author contributions: H.R. and P.T. designed research; H.R. performed research; H.R. analyzed data; H.R. and P.T. wrote the paper; and P.T. developed the conceptual framework and contributed to discussing analysis.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: Data for this article have been deposited at Figshare (https://figshare.com/articles/Dataset_Decoding_of_the_other_s_focus_of_attention_by_a_temporal_cortex_module/10265993).

  • See online for related content such as Commentaries.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1911269117/-/DCSupplemental.

Published under the PNAS license.

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Decoding of the other’s focus of attention by a temporal cortex module
Hamidreza Ramezanpour, Peter Thier
Proceedings of the National Academy of Sciences Feb 2020, 117 (5) 2663-2670; DOI: 10.1073/pnas.1911269117

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Decoding of the other’s focus of attention by a temporal cortex module
Hamidreza Ramezanpour, Peter Thier
Proceedings of the National Academy of Sciences Feb 2020, 117 (5) 2663-2670; DOI: 10.1073/pnas.1911269117
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