Inferential eye movement control while following dynamic gaze
Abstract
Attending to other people's gaze is evolutionary important to make inferences about intentions and actions. Gaze influences covert attention and triggers eye movements. However, we know little about how the brain controls the fine-grain dynamics of eye movements during gaze following. Observers followed people's gaze shifts in videos during search and we related the observer eye movement dynamics to the time course of gazer head movements extracted by a deep neural network. We show that the observers' brains use information in the visual periphery to execute predictive saccades that anticipate the information in the gazer's head direction by 190-350 ms. The brain simultaneously monitors moment-to-moment changes in the gazer's head velocity to dynamically alter eye movements and re-fixate the gazer (reverse saccades) when the head accelerates before the initiation of the first forward gaze-following saccade. Using saccade-contingent manipulations of the videos, we experimentally show that the reverse saccades are planned concurrently with the first forward gaze-following saccade and have a functional role in reducing subsequent errors fixating on the gaze goal. Together, our findings characterize the inferential and functional nature of social attention's fine-grain eye movement dynamics.
Data availability
All data generated or analyzed during this study are deposited at https://osf.io/g9bzt/
Article and author information
Author details
Funding
Army Research Office (W911NF-19-D-0001)
- Miguel Patricio Eckstein
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: The experiment protocol was approved by the University of California Internal Review Board with protocol number 12-22-0667. All participants signed consent forms to participate in the experiment and to include their images in resulting publications.
Copyright
© 2023, Han & Eckstein
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
-
- 560
- views
-
- 81
- downloads
-
- 1
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
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
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
-
- Neuroscience
Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.