Developmental maturation of causal signaling hubs in voluntary control of saccades and their functional controllability

Author:

Zhang Yuan12ORCID,Ryali Srikanth12,Cai Weidong12,Supekar Kaustubh12,Pasumarthy Ramkrishna34,Padmanabhan Aarthi12,Luna Bea5676,Menon Vinod12829

Affiliation:

1. Department of Psychiatry and Behavioral Sciences , , Stanford, CA 94305 , USA

2. Stanford University School of Medicine , , Stanford, CA 94305 , USA

3. Department of Electrical Engineering , , Chennai 600036 , India

4. Robert Bosch Center of Data Sciences and Artificial Intelligence, Network Systems Learning, Control and Evolution Group, Indian Institute of Technology Madras , , Chennai 600036 , India

5. Department of Psychiatry and Behavioral Sciences , , Pittsburgh, PA 15213 , USA

6. University of Pittsburgh , , Pittsburgh, PA 15213 , USA

7. Department of Psychology , , Pittsburgh, PA 15213 , USA

8. Department of Neurology & Neurological Sciences , , Stanford, CA 94305 , USA

9. Wu Tsai Neuroscience Institute, Stanford University School of Medicine , Stanford, CA 94305 , USA

Abstract

Abstract The ability to adaptively respond to behaviorally relevant cues in the environment, including voluntary control of automatic but inappropriate responses and deployment of a goal-relevant alternative response, undergoes significant maturation from childhood to adulthood. Importantly, the maturation of voluntary control processes influences the developmental trajectories of several key cognitive domains, including executive function and emotion regulation. Understanding the maturation of voluntary control is therefore of fundamental importance, but little is known about the underlying causal functional circuit mechanisms. Here, we use state-space and control-theoretic modeling to investigate the maturation of causal signaling mechanisms underlying voluntary control over saccades. We demonstrate that directed causal interactions in a canonical saccade network undergo significant maturation between childhood and adulthood. Crucially, we show that the frontal eye field (FEF) is an immature causal signaling hub in children during control over saccades. Using control-theoretic analysis, we then demonstrate that the saccade network is less controllable in children and that greater energy is required to drive FEF dynamics in children compared to adults. Our findings provide novel evidence that strengthening of causal signaling hubs and controllability of FEF are key mechanisms underlying age-related improvements in the ability to plan and execute voluntary control over saccades.

Funder

National Institutes of Health

Indo-U.S. Science and Technology Forum

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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