A unifying mechanism governing inter-brain neural relationship during social interactions
Abstract
A key goal of social neuroscience is to understand the inter-brain neural relationship - the relationship between the neural activity of socially interacting individuals. Decades of research investigating this relationship have focused on the similarity in neural activity across brains. Here we instead asked how neural activity differs between brains, and how that difference evolves alongside activity patterns shared between brains. Applying this framework to bats engaged in spontaneous social interactions revealed two complementary phenomena characterizing the inter-brain neural relationship: fast fluctuations of activity difference across brains unfolding in parallel with slow activity covariation across brains. A model reproduced these observations and generated multiple predictions that we confirmed using experimental data involving pairs of bats and a larger social group of bats. The model suggests that a simple computational mechanism involving positive and negative feedback could explain diverse experimental observations regarding the inter-brain neural relationship.
Data availability
Source code for the models is available at https://github.com/zhangwujie/Neurobat-lab-codes/tree/master/Interbrain-model
Article and author information
Author details
Funding
National Institutes of Health (DP2-DC016163)
- Michael M Yartsev
Dana Foundation
- Michael M Yartsev
National Institute of Mental Health (1-R01MH25387-01)
- Michael M Yartsev
New York Stem Cell Foundation (NYSCF-R-NI40)
- Michael M Yartsev
Alfred P. Sloan Foundation (FG-2017-9646)
- Michael M Yartsev
Brain Research Foundation (BRFSG-2017-09)
- Michael M Yartsev
National Science Foundation (NSF- 1550818)
- Michael M Yartsev
Packard Fellowship (2017-66825)
- Michael M Yartsev
Klingenstein-Simons Fellowship
- Michael M Yartsev
Pew Charitable Trust (00029645)
- Michael M Yartsev
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All experimental procedures complied with all relevant ethical regulations for animal testing and research and were approved by the Institutional Animal Care and Use Committee of the University of California, Berkeley (protocol number AUP-2015-01-7122-2).
Copyright
© 2022, Zhang et al.
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
-
- 1,911
- views
-
- 353
- downloads
-
- 4
- 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.