An approximate line attractor in the hypothalamus encodes an aggressive state

Creators: Nair, Aditya; Karigo, Tomomi; Yang, Bin; Ganguli, Surya; Schnitzer, Mark J.; Linderman, Scott W.; Anderson, David J.; Kennedy, Ann

Abstract

The hypothalamus regulates innate social behaviors, including mating and aggression. These behaviors can be evoked by optogenetic stimulation of specific neuronal subpopulations within MPOA and VMHvl, respectively. Here, we perform dynamical systems modeling of population neuronal activity in these nuclei during social behaviors. In VMHvl, unsupervised analysis identified a dominant dimension of neural activity with a large time constant (>50 s), generating an approximate line attractor in neural state space. Progression of the neural trajectory along this attractor was correlated with an escalation of agonistic behavior, suggesting that it may encode a scalable state of aggressiveness. Consistent with this, individual differences in the magnitude of the integration dimension time constant were strongly correlated with differences in aggressiveness. In contrast, approximate line attractors were not observed in MPOA during mating; instead, neurons with fast dynamics were tuned to specific actions. Thus, different hypothalamic nuclei employ distinct neural population codes to represent similar social behaviors.

Additional Information

Attribution 4.0 International (CC BY 4.0). We thank H. Inagaki and L.F. Abbott for critical feedback on this manuscript, C. Chiu for laboratory management, G. Mancuso for administrative assistance, and members of the Anderson and Kennedy labs for helpful comments on this project. A.N. is supported by a National Science Scholarship from the Agency for Science, Technology and Research, Singapore. D.J.A. is an investigator of the Howard Hughes Medical Institute. A.K. is supported by NIH R00MH117264. This work was supported in part by NIH grants NS123916, MH1223612, and MH070053 to D.J.A. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We support inclusive, diverse, and equitable conduct of research. We acknowledge that this research was conducted at Caltech, which is located on the unceded land of the Indigenous Tongva people. Author contributions. D.J.A., A.K., S.G., M.J.S., and A.N. conceived of the project. A.N., A.K., and D.J.A. wrote the manuscript, with input from T.K., B.Y., and S.W.L. A.K. performed the clustering analysis of single neurons and A.N. performed all dynamical system modeling. The authors declare no competing interests. Inclusion and diversity. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in their field of research or within their geographical location. While citing references scientifically relevant for this work, we also actively worked to promote gender balance in our reference list. Data and code availability: • Source data used in this paper will be shared by the lead contact upon request. • Code used for analyses in this paper is available in the following repositories: https://github.com/lindermanlab/ssm and https://github.com/DJALab/VMHvl_MPOA_dynamics • Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.

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