Multiplexing of cognitive encoding by oculomotor networks leads to incidental gaze shifts

Humans and other animals are adept at learning to perform cognitively demanding behavioral tasks. Neurophysiological recordings in nonhuman primates during such tasks find that the requisite cognitive variables are encoded strongly in core oculomotor brain regions. Here, we assembled a large dataset...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 122; no. 15; p. e2422331122
Main Authors Rosen, Matthew C., Freedman, David J.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 15.04.2025
Subjects
Animals
Classification
Cognition - physiology
Cognitive tasks
Eye
Eye movements
Eye Movements - physiology
Fixation, Ocular - physiology
Humans
Macaca mulatta
Male
Multiplexing
Oculomotor behavior
Primates
Saccades - physiology
Saccadic eye movements
Subspaces
Visual tasks
eye movements
parietal cortex
cognition
neurophysiology
working memory
Online AccessGet full text
ISSN0027-8424
1091-6490
1091-6490
DOI10.1073/pnas.2422331122

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Abstract Humans and other animals are adept at learning to perform cognitively demanding behavioral tasks. Neurophysiological recordings in nonhuman primates during such tasks find that the requisite cognitive variables are encoded strongly in core oculomotor brain regions. Here, we assembled a large dataset—11 monkeys performing an abstract visual categorization task, surveyed across more than 1,000 neural recording sessions—to reveal that this produces a robust but uninstructed behavioral “tell,” observed in all subjects and experiments: small, cognitively modulated eye movements. We find that these eye movements are causally linked to activity in SC but not LIP, and that they occur following transient alignment of cognitive and saccadic population coding subspaces in SC. This behavioral signature of oculomotor engagement is absent during a similar task that does not require rule-based categorization, suggesting that abstract task behaviors recruit primate oculomotor networks more strongly than previously understood.
AbstractList Humans and other animals are adept at learning to perform cognitively demanding behavioral tasks. Neurophysiological recordings in nonhuman primates during such tasks find that the requisite cognitive variables are encoded strongly in core oculomotor brain regions. Here, we assembled a large dataset-11 monkeys performing an abstract visual categorization task, surveyed across more than 1,000 neural recording sessions-to reveal that this produces a robust but uninstructed behavioral "tell," observed in all subjects and experiments: small, cognitively modulated eye movements. We find that these eye movements are causally linked to activity in SC but not LIP, and that they occur following transient alignment of cognitive and saccadic population coding subspaces in SC. This behavioral signature of oculomotor engagement is absent during a similar task that does not require rule-based categorization, suggesting that abstract task behaviors recruit primate oculomotor networks more strongly than previously understood.
Humans and other animals are adept at learning to perform cognitively demanding behavioral tasks. Neurophysiological recordings in nonhuman primates during such tasks find that the requisite cognitive variables are encoded strongly in core oculomotor brain regions. Here, we assembled a large dataset-11 monkeys performing an abstract visual categorization task, surveyed across more than 1,000 neural recording sessions-to reveal that this produces a robust but uninstructed behavioral "tell," observed in all subjects and experiments: small, cognitively modulated eye movements. We find that these eye movements are causally linked to activity in SC but not LIP, and that they occur following transient alignment of cognitive and saccadic population coding subspaces in SC. This behavioral signature of oculomotor engagement is absent during a similar task that does not require rule-based categorization, suggesting that abstract task behaviors recruit primate oculomotor networks more strongly than previously understood.Humans and other animals are adept at learning to perform cognitively demanding behavioral tasks. Neurophysiological recordings in nonhuman primates during such tasks find that the requisite cognitive variables are encoded strongly in core oculomotor brain regions. Here, we assembled a large dataset-11 monkeys performing an abstract visual categorization task, surveyed across more than 1,000 neural recording sessions-to reveal that this produces a robust but uninstructed behavioral "tell," observed in all subjects and experiments: small, cognitively modulated eye movements. We find that these eye movements are causally linked to activity in SC but not LIP, and that they occur following transient alignment of cognitive and saccadic population coding subspaces in SC. This behavioral signature of oculomotor engagement is absent during a similar task that does not require rule-based categorization, suggesting that abstract task behaviors recruit primate oculomotor networks more strongly than previously understood.
Author Freedman, David J.
Rosen, Matthew C.
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SubjectTerms Animals
Classification
Cognition - physiology
Cognitive tasks
Eye
Eye movements
Eye Movements - physiology
Fixation, Ocular - physiology
Humans
Macaca mulatta
Male
Multiplexing
Oculomotor behavior
Primates
Saccades - physiology
Saccadic eye movements
Subspaces
Visual tasks
Title Multiplexing of cognitive encoding by oculomotor networks leads to incidental gaze shifts
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