Tracking the Mind’s Eye: Primate Gaze Behavior during Virtual Visuomotor Navigation Reflects Belief Dynamics

To take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles underlying such belief updates, we need tools to uncover subjects’ belief dynamics from natural behavior. We tested whether eye movements could be use...

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Published inNeuron (Cambridge, Mass.) Vol. 106; no. 4; pp. 662 - 674.e5
Main Authors Lakshminarasimhan, Kaushik J., Avila, Eric, Neyhart, Erin, DeAngelis, Gregory C., Pitkow, Xaq, Angelaki, Dora E.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 20.05.2020
Elsevier Limited
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Online AccessGet full text
ISSN0896-6273
1097-4199
1097-4199
DOI10.1016/j.neuron.2020.02.023

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Abstract To take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles underlying such belief updates, we need tools to uncover subjects’ belief dynamics from natural behavior. We tested whether eye movements could be used to infer subjects’ beliefs about latent variables using a naturalistic navigation task. Humans and monkeys navigated to a remembered goal location in a virtual environment that provided optic flow but lacked explicit position cues. We observed eye movements that appeared to continuously track the goal location even when no visible target was present there. Accurate goal tracking was associated with improved task performance, and inhibiting eye movements in humans impaired navigation precision. These results suggest that gaze dynamics play a key role in action selection during challenging visuomotor behaviors and may possibly serve as a window into the subject’s dynamically evolving internal beliefs. •Humans and monkeys virtually navigated to a memorized goal by integrating optic flow•Eye movements tracked the goal location as subjects steered toward it•Better goal tracking was associated with better navigation performance•Forcing humans to fixate impaired navigation precision Humans and animals constantly maintain and update beliefs about latent world states, but those belief dynamics are notoriously difficult to measure experimentally. Using a naturalistic task in which subjects navigated to a hidden goal in virtual reality, Lakshminarasimhan et al. demonstrate that this could be achieved by tracking eye movements.
AbstractList To take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles underlying such belief updates, we need tools to uncover subjects’ belief dynamics from natural behaviour. We tested whether eye movements could be used to infer subjects’ beliefs about latent variables using a naturalistic navigation task. Humans and monkeys navigated to a remembered goal location in a virtual environment that provided optic flow but lacked explicit position cues. We observed eye movements that appeared to continuously track the goal location even when no visible target was present there. Accurate goal-tracking was associated with improved task performance, and inhibiting eye movements in humans impaired navigation precision. These results suggest that gaze dynamics play a key role in action-selection during challenging visuomotor behaviours, and may possibly serve as a window into the subject’s dynamically evolving internal beliefs. Humans and animals constantly maintain and update beliefs about latent world-states, but those belief dynamics are notoriously difficult to measure experimentally. Using a naturalistic task in which subjects navigated to a hidden goal in virtual reality, Lakshminarasimhan et al. demonstrate that this could be achieved by tracking eye movements.
To take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles underlying such belief updates, we need tools to uncover subjects’ belief dynamics from natural behavior. We tested whether eye movements could be used to infer subjects’ beliefs about latent variables using a naturalistic navigation task. Humans and monkeys navigated to a remembered goal location in a virtual environment that provided optic flow but lacked explicit position cues. We observed eye movements that appeared to continuously track the goal location even when no visible target was present there. Accurate goal tracking was associated with improved task performance, and inhibiting eye movements in humans impaired navigation precision. These results suggest that gaze dynamics play a key role in action selection during challenging visuomotor behaviors and may possibly serve as a window into the subject’s dynamically evolving internal beliefs. •Humans and monkeys virtually navigated to a memorized goal by integrating optic flow•Eye movements tracked the goal location as subjects steered toward it•Better goal tracking was associated with better navigation performance•Forcing humans to fixate impaired navigation precision Humans and animals constantly maintain and update beliefs about latent world states, but those belief dynamics are notoriously difficult to measure experimentally. Using a naturalistic task in which subjects navigated to a hidden goal in virtual reality, Lakshminarasimhan et al. demonstrate that this could be achieved by tracking eye movements.
To take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles underlying such belief updates, we need tools to uncover subjects' belief dynamics from natural behavior. We tested whether eye movements could be used to infer subjects' beliefs about latent variables using a naturalistic navigation task. Humans and monkeys navigated to a remembered goal location in a virtual environment that provided optic flow but lacked explicit position cues. We observed eye movements that appeared to continuously track the goal location even when no visible target was present there. Accurate goal tracking was associated with improved task performance, and inhibiting eye movements in humans impaired navigation precision. These results suggest that gaze dynamics play a key role in action selection during challenging visuomotor behaviors and may possibly serve as a window into the subject's dynamically evolving internal beliefs.To take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles underlying such belief updates, we need tools to uncover subjects' belief dynamics from natural behavior. We tested whether eye movements could be used to infer subjects' beliefs about latent variables using a naturalistic navigation task. Humans and monkeys navigated to a remembered goal location in a virtual environment that provided optic flow but lacked explicit position cues. We observed eye movements that appeared to continuously track the goal location even when no visible target was present there. Accurate goal tracking was associated with improved task performance, and inhibiting eye movements in humans impaired navigation precision. These results suggest that gaze dynamics play a key role in action selection during challenging visuomotor behaviors and may possibly serve as a window into the subject's dynamically evolving internal beliefs.
To take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles underlying such belief updates, we need tools to uncover subjects' belief dynamics from natural behavior. We tested whether eye movements could be used to infer subjects' beliefs about latent variables using a naturalistic navigation task. Humans and monkeys navigated to a remembered goal location in a virtual environment that provided optic flow but lacked explicit position cues. We observed eye movements that appeared to continuously track the goal location even when no visible target was present there. Accurate goal tracking was associated with improved task performance, and inhibiting eye movements in humans impaired navigation precision. These results suggest that gaze dynamics play a key role in action selection during challenging visuomotor behaviors and may possibly serve as a window into the subject's dynamically evolving internal beliefs.
SummaryTo take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles underlying such belief updates, we need tools to uncover subjects’ belief dynamics from natural behavior. We tested whether eye movements could be used to infer subjects’ beliefs about latent variables using a naturalistic navigation task. Humans and monkeys navigated to a remembered goal location in a virtual environment that provided optic flow but lacked explicit position cues. We observed eye movements that appeared to continuously track the goal location even when no visible target was present there. Accurate goal tracking was associated with improved task performance, and inhibiting eye movements in humans impaired navigation precision. These results suggest that gaze dynamics play a key role in action selection during challenging visuomotor behaviors and may possibly serve as a window into the subject’s dynamically evolving internal beliefs.
Author Lakshminarasimhan, Kaushik J.
Neyhart, Erin
Pitkow, Xaq
Avila, Eric
DeAngelis, Gregory C.
Angelaki, Dora E.
AuthorAffiliation 6 Tandon school of Engineering, New York University, New York, NY, USA
2 Center for Theoretical Neuroscience, Columbia University, New York, NY, USA
7 These authors contributed equally
3 Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA
4 Brain and Cognitive Sciences, University of Rochester, Rochester, NY, USA
5 Department of Electrical and Computer Engineering, Rice University, Houston, TX, USA
1 Center for Neural Science, New York University, New York, NY, USA
AuthorAffiliation_xml – name: 1 Center for Neural Science, New York University, New York, NY, USA
– name: 5 Department of Electrical and Computer Engineering, Rice University, Houston, TX, USA
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– name: 4 Brain and Cognitive Sciences, University of Rochester, Rochester, NY, USA
– name: 7 These authors contributed equally
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AUTHOR CONTRIBUTIONS
Conceptualization, K.J.L., G.C.D., X.P. and D.E.A.; Methodology, K.J.L., E.A., X.P. and D.E.A., Investigation, K.J.L., E.A. and E.N.; Data Curation, K.J.L. and E.A.; Formal Analysis, K.J.L.; Writing - Original draft, K.J.L.; Writing - Review & Editing, K.J.L., E.A., G.C.D., X.P. and D.E.A.; Funding Acquisition - G.C.D., X.P. and D.E.A.; Supervision, X.P. and D.E.A.
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Snippet To take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles...
SummaryTo take the best actions, we often need to maintain and update beliefs about variables that cannot be directly observed. To understand the principles...
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pubmed
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SubjectTerms Adolescent
Adult
Animals
Behavior
Decision Making - physiology
Eye
Eye movements
Female
Fixation, Ocular - physiology
Human subjects
Humans
Macaca mulatta
Male
Models, Neurological
Navigation behavior
Oculomotor behavior
Optic flow
Sensorimotor integration
Spatial Navigation - physiology
Standard deviation
Young Adult
Title Tracking the Mind’s Eye: Primate Gaze Behavior during Virtual Visuomotor Navigation Reflects Belief Dynamics
URI https://dx.doi.org/10.1016/j.neuron.2020.02.023
https://www.ncbi.nlm.nih.gov/pubmed/32171388
https://www.proquest.com/docview/2425667731
https://www.proquest.com/docview/2377680628
https://pubmed.ncbi.nlm.nih.gov/PMC7323886
Volume 106
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