Unsupervised decomposition of natural monkey behavior into a sequence of motion motifs.

Koki Mimura, Jumpei Matsumoto, Daichi Mochihashi, Tomoaki Nakamura, Hisao Nishijo, Makoto Higuchi, Toshiyuki Hirabayashi, Takafumi Minamimoto
Author Information
  1. Koki Mimura: Advanced Neuroimaging Center, National Institutes for Quantum Science and Technology, Chiba, 263-8555, Japan. mimura.koki@qst.go.jp. ORCID
  2. Jumpei Matsumoto: Department of System Emotional Science, Faculty of Medicine, University of Toyama, Toyama, 930-8555, Japan.
  3. Daichi Mochihashi: Department of Statistical Inference and Mathematics, The Institute of Statistical Mathematics, Tokyo, 190-9562, Japan.
  4. Tomoaki Nakamura: Department of Mechanical Engineering and Intelligent Systems, The University of Electro-Communications, Tokyo, 182-8585, Japan.
  5. Hisao Nishijo: Department of System Emotional Science, Faculty of Medicine, University of Toyama, Toyama, 930-8555, Japan.
  6. Makoto Higuchi: Advanced Neuroimaging Center, National Institutes for Quantum Science and Technology, Chiba, 263-8555, Japan.
  7. Toshiyuki Hirabayashi: Advanced Neuroimaging Center, National Institutes for Quantum Science and Technology, Chiba, 263-8555, Japan.
  8. Takafumi Minamimoto: Advanced Neuroimaging Center, National Institutes for Quantum Science and Technology, Chiba, 263-8555, Japan. minamimoto.takafumi@qst.go.jp. ORCID

Abstract

Nonhuman primates (NHPs) exhibit complex and diverse behavior that typifies advanced cognitive function and social communication, but quantitative and systematical measure of this natural nonverbal processing has been a technical challenge. Specifically, a method is required to automatically segment time series of behavior into elemental motion motifs, much like finding meaningful words in character strings. Here, we propose a solution called SyntacticMotionParser (SMP), a general-purpose unsupervised behavior parsing algorithm using a nonparametric Bayesian model. Using three-dimensional posture-tracking data from NHPs, SMP automatically outputs an optimized sequence of latent motion motifs classified into the most likely number of states. When applied to behavioral datasets from common marmosets and rhesus monkeys, SMP outperformed conventional posture-clustering models and detected a set of behavioral ethograms from publicly available data. SMP also quantified and visualized the behavioral effects of chemogenetic neural manipulations. SMP thus has the potential to dramatically improve our understanding of natural NHP behavior in a variety of contexts.

References

  1. Neuron. 2015 Dec 16;88(6):1121-1135 [PMID: 26687221]
  2. Nat Neurosci. 2022 Feb;25(2):201-212 [PMID: 35132235]
  3. Curr Opin Neurobiol. 2020 Feb;60:1-11 [PMID: 31791006]
  4. J Neurosci Methods. 2014 Aug 30;234:147-52 [PMID: 24875622]
  5. Nat Neurosci. 2019 Dec;22(12):2040-2049 [PMID: 31768056]
  6. iScience. 2021 Aug 30;24(9):103066 [PMID: 34568790]
  7. Neurosci Biobehav Rev. 2020 Aug;115:378-395 [PMID: 31991191]
  8. Nat Commun. 2021 May 13;12(1):2784 [PMID: 33986265]
  9. Genes Brain Behav. 2019 Jan;18(1):e12544 [PMID: 30549185]
  10. IEEE Trans Pattern Anal Mach Intell. 2008 Feb;30(2):283-98 [PMID: 18084059]
  11. Neuropsychopharmacology. 2009 Jan;34(1):90-105 [PMID: 18800061]
  12. Front Neurorobot. 2017 Dec 21;11:67 [PMID: 29311889]
  13. Nat Commun. 2021 Sep 15;12(1):5388 [PMID: 34526497]
  14. Proc Natl Acad Sci U S A. 2020 Sep 29;117(39):24022-24031 [PMID: 32817435]
  15. Nature. 2020 Jan;577(7789):239-243 [PMID: 31853063]
  16. Nat Methods. 2022 Apr;19(4):496-504 [PMID: 35414125]
  17. Cell Rep. 2018 Aug 21;24(8):2191-2195.e4 [PMID: 30134178]
  18. Nat Commun. 2020 Sep 11;11(1):4560 [PMID: 32917899]
  19. Commun Biol. 2022 Nov 18;5(1):1267 [PMID: 36400882]
  20. PLoS Biol. 2018 Feb 27;16(2):e2004825 [PMID: 29485994]
  21. Curr Opin Neurobiol. 2021 Oct;70:89-100 [PMID: 34482006]
  22. J Neurosci. 2022 Aug 10;42(32):6267-6275 [PMID: 35794012]
  23. Front Behav Neurosci. 2021 Jan 18;14:581154 [PMID: 33584214]
  24. J R Soc Interface. 2014 Oct 6;11(99): [PMID: 25142523]
  25. PLoS One. 2013 Oct 30;8(10):e78460 [PMID: 24205238]
  26. Curr Biol. 2022 Aug 8;32(15):3423-3428.e3 [PMID: 35750054]
  27. Elife. 2021 Nov 30;10: [PMID: 34846301]
  28. Curr Opin Neurobiol. 2022 Jun;74:102549 [PMID: 35537373]
  29. Anim Cogn. 2018 Sep;21(5):619-629 [PMID: 29876698]
  30. Curr Biol. 2022 May 23;32(10):R482-R493 [PMID: 35609550]
  31. Nat Neurosci. 2020 Nov;23(11):1433-1443 [PMID: 32958923]
  32. Neuron. 2019 Jan 16;101(2):307-320.e6 [PMID: 30528065]
  33. Sci Adv. 2021 Jun 23;7(26): [PMID: 34162548]
  34. J Neurosci. 2004 Jan 21;24(3):711-21 [PMID: 14736857]
  35. Exp Neurol. 2018 Jan;299(Pt A):252-265 [PMID: 28774750]
  36. Curr Biol. 2022 Mar 28;32(6):1211-1231.e7 [PMID: 35139360]
  37. Mol Ther. 2021 Dec 1;29(12):3484-3497 [PMID: 33895327]

Grants

  1. JP19H04996/MEXT | Japan Society for the Promotion of Science (JSPS)
  2. 22K07338/MEXT | Japan Society for the Promotion of Science (JSPS)
  3. 22H05157/MEXT | Japan Society for the Promotion of Science (JSPS)
  4. JP24H00069/MEXT | Japan Society for the Promotion of Science (JSPS)
  5. JP20dm0207072/Japan Agency for Medical Research and Development (AMED)
  6. JP20dm0307007/Japan Agency for Medical Research and Development (AMED)
  7. JP20dm0107146/Japan Agency for Medical Research and Development (AMED)

MeSH Term

Animals
Behavior, Animal
Macaca mulatta
Bayes Theorem
Algorithms
Callithrix
Male

Word Cloud

Created with Highcharts 10.0.0behaviorSMPnaturalmotionmotifsbehavioralNHPsautomaticallydatasequenceNonhumanprimatesexhibitcomplexdiversetypifiesadvancedcognitivefunctionsocialcommunicationquantitativesystematicalmeasurenonverbalprocessingtechnicalchallengeSpecificallymethodrequiredsegmenttimeserieselementalmuchlikefindingmeaningfulwordscharacterstringsproposesolutioncalledSyntacticMotionParsergeneral-purposeunsupervisedparsingalgorithmusingnonparametricBayesianmodelUsingthree-dimensionalposture-trackingoutputsoptimizedlatentclassifiedlikelynumberstatesapplieddatasetscommonmarmosetsrhesusmonkeysoutperformedconventionalposture-clusteringmodelsdetectedsetethogramspubliclyavailablealsoquantifiedvisualizedeffectschemogeneticneuralmanipulationsthuspotentialdramaticallyimproveunderstandingNHPvarietycontextsUnsuperviseddecompositionmonkey

Similar Articles

Cited By