Space wandering in the rodent default mode network

Author:

Nghiem Trang-Anh Estelle1ORCID,Lee Byeongwook1,Chao Tzu-Hao Harry234,Branigan Nicholas K.1,Mistry Percy K.1ORCID,Shih Yen-Yu Ian2345ORCID,Menon Vinod167

Affiliation:

1. Department of Psychiatry & Behavioral Sciences, Stanford University, Palo Alto, CA 94304

2. Center for Animal MRI, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599

3. Biomedical Research Imaging Center, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599

4. Department of Neurology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599

5. Department of Biomedical Engineering, University of North Carolina at Chapel Hill, Chapel Hill, NC 27514

6. Department of Neurology & Neurological Sciences, Stanford University, Palo Alto, CA 94304

7. Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA 94305

Abstract

The default mode network (DMN) is a large-scale brain network known to be suppressed during a wide range of cognitive tasks. However, our comprehension of its role in naturalistic and unconstrained behaviors has remained elusive because most research on the DMN has been conducted within the restrictive confines of MRI scanners. Here, we use multisite GCaMP (a genetically encoded calcium indicator) fiber photometry with simultaneous videography to probe DMN function in awake, freely exploring rats. We examined neural dynamics in three core DMN nodes—the retrosplenial cortex, cingulate cortex, and prelimbic cortex—as well as the anterior insula node of the salience network, and their association with the rats’ spatial exploration behaviors. We found that DMN nodes displayed a hierarchical functional organization during spatial exploration, characterized by stronger coupling with each other than with the anterior insula. Crucially, these DMN nodes encoded the kinematics of spatial exploration, including linear and angular velocity. Additionally, we identified latent brain states that encoded distinct patterns of time-varying exploration behaviors and found that higher linear velocity was associated with enhanced DMN activity, heightened synchronization among DMN nodes, and increased anticorrelation between the DMN and anterior insula. Our findings highlight the involvement of the DMN in collectively and dynamically encoding spatial exploration in a real-world setting. Our findings challenge the notion that the DMN is primarily a “task-negative” network disengaged from the external world. By illuminating the DMN’s role in naturalistic behaviors, our study underscores the importance of investigating brain network function in ecologically valid contexts.

Funder

HHS | NIH | National Institute of Mental Health

HHS | NIH | National Institute of Neurological Disorders and Stroke

HHS | NIH | National Institute on Alcohol Abuse and Alcoholism

HHS | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development

HHS | NIH | NIH Office of the Director

Publisher

Proceedings of the National Academy of Sciences

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