Unsupervised Identification of the Internal States That Shape Natural Behavior

Overview

Journal Nat Neurosci

Date 2019 Nov 27

PMID 31768056

Citations 86

Authors

Adam J Calhoun

Jonathan W Pillow

Mala Murthy

Affiliations

Soon will be listed here.

Abstract

Internal states shape stimulus responses and decision-making, but we lack methods to identify them. To address this gap, we developed an unsupervised method to identify internal states from behavioral data and applied it to a dynamic social interaction. During courtship, Drosophila melanogaster males pattern their songs using feedback cues from their partner. Our model uncovers three latent states underlying this behavior and is able to predict moment-to-moment variation in song-patterning decisions. These states correspond to different sensorimotor strategies, each of which is characterized by different mappings from feedback cues to song modes. We show that a pair of neurons previously thought to be command neurons for song production are sufficient to drive switching between states. Our results reveal how animals compose behavior from previously unidentified internal states, which is a necessary step for quantitative descriptions of animal behavior that link environmental cues, internal needs, neuronal activity and motor outputs.

Citing Articles

Historical loss weakens competitive behavior by remodeling ventral hippocampal dynamics.

Lai C, Chen K, Huang H, Huang X, Zhang J, Wang Y Cell Discov. 2025; 11(1):16.

PMID: 39994206 PMC: 11850767. DOI: 10.1038/s41421-024-00751-3.

Deciphering neuronal variability across states reveals dynamic sensory encoding.

Akella S, Ledochowitsch P, Siegle J, Belski H, Denman D, Buice M Nat Commun. 2025; 16(1):1768.

PMID: 39971911 PMC: 11839951. DOI: 10.1038/s41467-025-56733-w.

In vivo electrophysiology recordings and computational modeling can predict octopus arm movement.

Gedela N, Radawiec R, Salim S, Richie J, Chestek C, Draelos A Bioelectron Med. 2025; 11(1):4.

PMID: 39948616 PMC: 11827351. DOI: 10.1186/s42234-025-00166-9.

Modeling Complex Animal Behavior with Latent State Inverse Reinforcement Learning.

Jha A, Geadah V, Pillow J bioRxiv. 2024; .

PMID: 39605387 PMC: 11601398. DOI: 10.1101/2024.11.13.623515.

Mesoscale neuronal granular trial variability in vivo illustrated by nonlinear recurrent network in silico.

Xiao G, Cai Y, Zhang Y, Xie J, Wu L, Xie H Nat Commun. 2024; 15(1):9894.

PMID: 39548098 PMC: 11567969. DOI: 10.1038/s41467-024-54346-3.

References

Berman G . Measuring behavior across scales. BMC Biol. 2018; 16(1):23. PMC: 5824583. DOI: 10.1186/s12915-018-0494-7. View

Calhoun A, Murthy M . Quantifying behavior to solve sensorimotor transformations: advances from worms and flies. Curr Opin Neurobiol. 2017; 46:90-98. PMC: 5765764. DOI: 10.1016/j.conb.2017.08.006. View

Egnor S, Branson K . Computational Analysis of Behavior. Annu Rev Neurosci. 2016; 39:217-36. DOI: 10.1146/annurev-neuro-070815-013845. View

Anderson D . Circuit modules linking internal states and social behaviour in flies and mice. Nat Rev Neurosci. 2016; 17(11):692-704. DOI: 10.1038/nrn.2016.125. View

Musall S, Kaufman M, Juavinett A, Gluf S, Churchland A . Single-trial neural dynamics are dominated by richly varied movements. Nat Neurosci. 2019; 22(10):1677-1686. PMC: 6768091. DOI: 10.1038/s41593-019-0502-4. View

Saleem A, Ayaz A, Jeffery K, Harris K, Carandini M . Integration of visual motion and locomotion in mouse visual cortex. Nat Neurosci. 2013; 16(12):1864-9. PMC: 3926520. DOI: 10.1038/nn.3567. View

Suver M, Mamiya A, Dickinson M . Octopamine neurons mediate flight-induced modulation of visual processing in Drosophila. Curr Biol. 2012; 22(24):2294-302. DOI: 10.1016/j.cub.2012.10.034. View

Liu M, Sharma A, Shaevitz J, Leifer A . Temporal processing and context dependency in response to mechanosensation. Elife. 2018; 7. PMC: 6054533. DOI: 10.7554/eLife.36419. View

Remedios R, Kennedy A, Zelikowsky M, Grewe B, Schnitzer M, Anderson D . Social behaviour shapes hypothalamic neural ensemble representations of conspecific sex. Nature. 2017; 550(7676):388-392. PMC: 5674977. DOI: 10.1038/nature23885. View

10.

Zhang S, Miner L, Boutros C, Rogulja D, Crickmore M . Motivation, Perception, and Chance Converge to Make a Binary Decision. Neuron. 2018; 99(2):376-388.e6. PMC: 7476641. DOI: 10.1016/j.neuron.2018.06.014. View

11.

Hoopfer E, Jung Y, Inagaki H, Rubin G, Anderson D . P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila. Elife. 2015; 4. PMC: 4749567. DOI: 10.7554/eLife.11346. View

12.

Leinwand S, Chalasani S . Neuropeptide signaling remodels chemosensory circuit composition in Caenorhabditis elegans. Nat Neurosci. 2013; 16(10):1461-7. PMC: 3786745. DOI: 10.1038/nn.3511. View

13.

Root C, Masuyama K, Green D, Enell L, Nassel D, Lee C . A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron. 2008; 59(2):311-21. PMC: 2539065. DOI: 10.1016/j.neuron.2008.07.003. View

14.

Iigaya K, Fonseca M, Murakami M, Mainen Z, Dayan P . An effect of serotonergic stimulation on learning rates for rewards apparent after long intertrial intervals. Nat Commun. 2018; 9(1):2477. PMC: 6018802. DOI: 10.1038/s41467-018-04840-2. View

15.

Grundemann J, Bitterman Y, Lu T, Krabbe S, Grewe B, Schnitzer M . Amygdala ensembles encode behavioral states. Science. 2019; 364(6437). DOI: 10.1126/science.aav8736. View

16.

Dietrich M, Zimmer M, Bober J, Horvath T . Hypothalamic Agrp neurons drive stereotypic behaviors beyond feeding. Cell. 2015; 160(6):1222-32. PMC: 4484787. DOI: 10.1016/j.cell.2015.02.024. View

17.

Wiltschko A, Johnson M, Iurilli G, Peterson R, Katon J, Pashkovski S . Mapping Sub-Second Structure in Mouse Behavior. Neuron. 2015; 88(6):1121-1135. PMC: 4708087. DOI: 10.1016/j.neuron.2015.11.031. View

18.

Katsov A, Freifeld L, Horowitz M, Kuehn S, Clandinin T . Dynamic structure of locomotor behavior in walking fruit flies. Elife. 2017; 6. PMC: 5526672. DOI: 10.7554/eLife.26410. View

19.

Corrado G, Sugrue L, Seung H, Newsome W . Linear-Nonlinear-Poisson models of primate choice dynamics. J Exp Anal Behav. 2006; 84(3):581-617. PMC: 1389782. DOI: 10.1901/jeab.2005.23-05. View

20.

Coen P, Clemens J, Weinstein A, Pacheco D, Deng Y, Murthy M . Dynamic sensory cues shape song structure in Drosophila. Nature. 2014; 507(7491):233-7. DOI: 10.1038/nature13131. View