Simple Behavioral Analysis (SimBA) as a platform for explainable machine learning in behavioral neuroscience

Machine Learning


  • Krakauer, J. W., Ghazanfar, A. A., Gomez-Marin, A., MacIver, M. A. & Poeppel, D. Neuroscience needs behavior: correcting a reductionist bias. Neuron 93, 480–490 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Anderson, D. J. & Perona, P. Toward a science of computational ethology. Neuron 84, 18–31 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Egnor, S. E. R. & Branson, K. Computational analysis of behavior. Annu. Rev. Neurosci. 39, 217–236 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Datta, S. R., Anderson, D. J., Branson, K., Perona, P. & Leifer, A. Computational neuroethology: a call to action. Neuron 104, 11–24 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Falkner, A. L., Grosenick, L., Davidson, T. J., Deisseroth, K. & Lin, D. Hypothalamic control of male aggression-seeking behavior. Nat. Neurosci. 19, 596–604 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ferenczi, E. A. et al. Prefrontal cortical regulation of brainwide circuit dynamics and reward-related behavior. Science 351, aac9698 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kim, Y. et al. Mapping social behavior-induced brain activation at cellular resolution in the mouse. Cell Rep. 10, 292–305 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Gunaydin, L. A. et al. Natural neural projection dynamics underlying social behavior. Cell 157, 1535–1551 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Graving, J. M. et al. DeepPoseKit, a software toolkit for fast and robust animal pose estimation using deep learning. eLife 8, e47994 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mathis, A. et al. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat. Neurosci. 21, 1281–1289 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Pereira, T. D. et al. Fast animal pose estimation using deep neural networks. Nat. Methods 16, 117–125 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Geuther, B. Q. et al. Robust mouse tracking in complex environments using neural networks. Commun. Biol. 2, 124 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gris, K. V., Coutu, J.-P. & Gris, D. Supervised and unsupervised learning technology in the study of rodent behavior. Front. Behav. Neurosci. 11, 141 (2017).

  • Schaefer, A. T. & Claridge-Chang, A. The surveillance state of behavioral automation. Curr. Opin. Neurobiol. 22, 170–176 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Robie, A. A., Seagraves, K. M., Egnor, S. E. R. & Branson, K. Machine vision methods for analyzing social interactions. J. Exp. Biol. 220, 25–34 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Vu, M.-A. T. et al. A shared vision for machine learning in neuroscience. J. Neurosci. 38, 1601–1607 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Goodwin, N. L., Nilsson, S. R. O., Choong, J. J. & Golden, S. A. Toward the explainability, transparency, and universality of machine learning for behavioral classification in neuroscience. Curr. Opin. Neurobiol. 73, 102544 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Newton, K. C. et al. Lateral line ablation by ototoxic compounds results in distinct rheotaxis profiles in larval zebrafish. Commun. Biol. 6, 1–15 (2023).

    Article 

    Google Scholar 

  • Jernigan, C. M., Stafstrom, J. A., Zaba, N. C., Vogt, C. C. & Sheehan, M. J. Color is necessary for face discrimination in the Northern paper wasp, Polistes fuscatus. Anim. Cogn. 26, 589–598 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dahake, A. et al. Floral humidity as a signal – not a cue – in a nocturnal pollination system. Preprint at bioRxiv https://doi.org/10.1101/2022.04.27.489805 (2022).

  • Dawson, M. et al. Hypocretin/orexin neurons encode social discrimination and exhibit a sex-dependent necessity for social interaction. Cell Rep. 42, 112815 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Baleisyte, A., Schneggenburger, R. & Kochubey, O. Stimulation of medial amygdala GABA neurons with kinetically different channelrhodopsins yields opposite behavioral outcomes. Cell Rep. 39, 110850 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Cruz-Pereira, J. S. et al. Prebiotic supplementation modulates selective effects of stress on behavior and brain metabolome in aged mice. Neurobiol. Stress 21, 100501 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Linders, L. E. et al. Stress-driven potentiation of lateral hypothalamic synapses onto ventral tegmental area dopamine neurons causes increased consumption of palatable food. Nat. Commun. 13, 6898 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Slivicki, R. A. et al. Oral oxycodone self-administration leads to features of opioid misuse in male and female mice. Addiction Biol. 28, e13253 (2023).

    Article 
    CAS 

    Google Scholar 

  • Miczek, K. A. et al. Excessive alcohol consumption after exposure to two types of chronic social stress: intermittent episodes vs. continuous exposure in C57BL/6J mice with a history of drinking. Psychopharmacology (Berl.) 239, 3287–3296 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Cui, Q. et al. Striatal direct pathway targets Npas1+ pallidal neurons. J. Neurosci. 41, 3966–3987 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chen, J. et al. A MYT1L syndrome mouse model recapitulates patient phenotypes and reveals altered brain development due to disrupted neuronal maturation. Neuron 109, 3775–3792 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rigney, N., Zbib, A., de Vries, G. J. & Petrulis, A. Knockdown of sexually differentiated vasopressin expression in the bed nucleus of the stria terminalis reduces social and sexual behaviour in male, but not female, mice. J. Neuroendocrinol. 34, e13083 (2021).

  • Winters, C. et al. Automated procedure to assess pup retrieval in laboratory mice. Sci. Rep. 12, 1663 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Neira, S. et al. Chronic alcohol consumption alters home-cage behaviors and responses to ethologically relevant predator tasks in mice. Alcohol Clin. Exp. Res. 46, 1616–1629 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kwiatkowski, C. C. et al. Quantitative standardization of resident mouse behavior for studies of aggression and social defeat. Neuropsychopharmacology 46, 1584–1593 (2021).

  • Yamaguchi, T. et al. Posterior amygdala regulates sexual and aggressive behaviors in male mice. Nat. Neurosci. 23, 1111–1124 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nygaard, K. R. et al. Extensive characterization of a Williams syndrome murine model shows Gtf2ird1-mediated rescue of select sensorimotor tasks, but no effect on enhanced social behavior. Genes Brain Behav. 22, e12853 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ojanen, S. et al. Interneuronal GluK1 kainate receptors control maturation of GABAergic transmission and network synchrony in the hippocampus. Mol. Brain 16, 43 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hon, O. J. et al. Serotonin modulates an inhibitory input to the central amygdala from the ventral periaqueductal gray. Neuropsychopharmacology 47, 2194–2204 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Murphy, C. A. et al. Modeling features of addiction with an oral oxycodone self-administration paradigm. Preprint at bioRxiv https://doi.org/10.1101/2021.02.08.430180 (2021).

  • Neira, S. et al. Impact and role of hypothalamic corticotropin releasing hormone neurons in withdrawal from chronic alcohol consumption in female and male mice. J. Neurosci. 43, 7657–7667 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lapp, H. E., Salazar, M. G. & Champagne, F. A. Automated maternal behavior during early life in rodents (AMBER) pipeline. Sci. Rep. 13, 18277 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Barnard, I. L. et al. High-THC cannabis smoke impairs incidental memory capacity in spontaneous tests of novelty preference for objects and odors in male rats. eNeuro 10, ENEURO.0115-23.2023 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ausra, J. et al. Wireless battery free fully implantable multimodal recording and neuromodulation tools for songbirds. Nat. Commun. 12, 1968 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Friard, O. & Gamba, M. BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol. Evol. 7, 1325–1330 (2016).

    Article 

    Google Scholar 

  • Spink, A. J., Tegelenbosch, R. A. J., Buma, M. O. S. & Noldus, L. P. J. J. The EthoVision video tracking system—a tool for behavioral phenotyping of transgenic mice. Physiol. Behav. 73, 731–744 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Lundberg, S. shap. https://github.com/shap/shap

  • Lauer, J. et al. Multi-animal pose estimation, identification and tracking with DeepLabCut. Nat. Methods 19, 496–504 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pereira, T. D. et al. SLEAP: a deep learning system for multi-animal pose tracking. Nat Methods 19, 486–495 (2022).

  • Segalin, C. et al. The Mouse Action Recognition System (MARS) software pipeline for automated analysis of social behaviors in mice. eLife 10, e63720 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Breiman, L. Random forests. Mach. Learn. 45, 5–32 (2001).

    Article 

    Google Scholar 

  • Liaw, A. & Wiener, M. Classification and regression by randomForest. R News 2/3 https://journal.r-project.org/articles/RN-2002-022/RN-2002-022.pdf (2022).

  • Goodwin, N. L., Nilsson, S. R. O. & Golden, S. A. Rage against the machine: advancing the study of aggression ethology via machine learning. Psychopharmacology 237, 2569–2588 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lundberg, S. M. et al. From local explanations to global understanding with explainable AI for trees. Nat. Mach. Intell. 2, 56–67 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ribeiro, M. T., Singh, S., & Guestrin, C. ‘Why should I trust you?’: explaining the predictions of any classifier. Preprint at arXiv https://doi.org/10.48550/arXiv.1602.04938 (2016).

  • Sundararajan, M., Taly, A. & Yan, Q. Axiomatic attribution for deep networks. In Proc. of the 34th International Conference on Machine Learning 3319–3328 (MLR Press, 2017).

  • Hatwell, J., Gaber, M. M. & Azad, R. M. A. CHIRPS: explaining random forest classification. Artif. Intell. Rev. 53, 5747–5788 (2020).

    Article 

    Google Scholar 

  • Lundberg, S. & Lee, S.-I. A unified approach to interpreting model predictions. Preprint at arXiv https://doi.org/10.48550/arXiv.1705.07874 (2017).

  • Verma, S., Dickerson, J. & Hines, K. Counterfactual explanations for machine learning: a review. Preprint at arXiv https://doi.org/10.48550/arXiv.2010.10596 (2020).

  • Rudin, C. Stop explaining black box machine learning models for high stakes decisions and use interpretable models instead. Nat. Mach. Intell. 1, 206–215 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Takahashi, A. et al. Establishment of a repeated social defeat stress model in female mice. Sci. Rep. 7, 12838 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hashikawa, K. et al. Esr1+ cells in the ventromedial hypothalamus control female aggression. Nat. Neurosci. 20, 1580–1590 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Newman, E. L. et al. Fighting females: neural and behavioral consequences of social defeat stress in female mice. Biol. Psychiatry 86, 657–668 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Aubry, A. V. et al. Sex differences in appetitive and reactive aggression. Neuropsychopharmacology 47, 1746–1754 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Golden, S. A., Covington, H. E., Berton, O. & Russo, S. J. A standardized protocol for repeated social defeat stress in mice. Nat. Protoc. 6, 1183–1191 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Shemesh, Y. & Chen, A. A paradigm shift in translational psychiatry through rodent neuroethology. Mol. Psychiatry 28, 993–1003 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kabra, M., Robie, A. A., Rivera-Alba, M., Branson, S. & Branson, K. JAABA: interactive machine learning for automatic annotation of animal behavior. Nat. Methods 10, 64–67 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Bordes, J. et al. Automatically annotated motion tracking identifies a distinct social behavioral profile following chronic social defeat stress. Nat. Commun. 14, 4319 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Winters, C., Gorssen, W., Wöhr, M. & D’Hooge, R. BAMBI: a new method for automated assessment of bidirectional early-life interaction between maternal behavior and pup vocalization in mouse dam-pup dyads. Front. Behav. Neurosci. 17, 1139254 (2023).

  • Lundberg, S. M., Erion, G. G. & Lee, S.-I. Consistent individualized feature attribution for tree ensembles. Preprint at arXiv https://doi.org/10.48550/arXiv.1802.03888 (2019).

  • Covert, I. C., Lundberg, S. & Lee, S.-I. Explaining by removing: a unified framework for model explanation. J. Mach. Learn. Res. 22, 1–90 (2021).

  • Lorbach, M., Poppe, R. & Veltkamp, R. C. Interactive rodent behavior annotation in video using active learning. Multimed. Tools Appl. 78, 19787–19806 (2019).

    Article 

    Google Scholar 

  • Tillmann, J. F., Hsu, A. I., Schwarz, M. K. & Yttri, E. A. A-SOiD, an active-learning platform for expert-guided, data-efficient discovery of behavior. Nat. Methods 21, 703–711 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Whiteway, M. R. et al. Partitioning variability in animal behavioral videos using semi-supervised variational autoencoders. PLoS Comput. Biol. 17, e1009439 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sun, J. J. et al. Task Programming: Learning Data Efficient Behavior Representations. In Proc IEEE Comput. Soc. Conf. Comput. Vis. Pattern Recognit. 2875–2884 (2021).

  • MABe 2022. Multi-agent behavior: representation, modeling, measurement, and applications. https://sites.google.com/view/mabe22/home

  • Sun, J. J. et al. The multi-agent behavior dataset: mouse dyadic social interactions. Preprint at arXiv https://doi.org/10.48550/arXiv.2104.02710 (2021).

  • OpenBehavior. About the OpenBehavior Project and the open source movement. https://edspace.american.edu/openbehavior/

  • Mouse Phenome Database. https://phenome.jax.org/about

  • Kapoor, S. & Narayanan, A. Leakage and the reproducibility crisis in machine-learning-based science. Patterns (N Y) 4, 100804 (2023).

    Article 
    PubMed 

    Google Scholar 

  • Dankert, H., Wang, L., Hoopfer, E. D., Anderson, D. J. & Perona, P. Automated monitoring and analysis of social behavior in Drosophila. Nat. Methods 6, 297–303 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • de Chaumont, F. et al. Real-time analysis of the behaviour of groups of mice via a depth-sensing camera and machine learning. Nat. Biomed. Eng. 3, 930–942 (2019).

    Article 
    PubMed 

    Google Scholar 

  • Giancardo, L. et al. Automatic visual tracking and social behaviour analysis with multiple mice. PLoS ONE 8, e74557 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hong, W. et al. Automated measurement of mouse social behaviors using depth sensing, video tracking, and machine learning. Proc. Natl Acad. Sci. USA 112, E5351–E5360 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Goodwin, N. L. et al. Simple behavioral analysis (SimBA) as a platform for explainable machine learning in behavioral neuroscience. Nat. Neurosci. (in the press).

  • Bohnslav, J. P. et al. DeepEthogram, a machine learning pipeline for supervised behavior classification from raw pixels. eLife 10, e63377 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gerós, A., Magalhães, A. & Aguiar, P. Improved 3D tracking and automated classification of rodents’ behavioral activity using depth-sensing cameras. Behav. Res. 52, 2156–2167 (2020).

    Article 

    Google Scholar 

  • Harris, C., Finn, K. R., Kieseler, M.-L., Maechler, M. R. & Tse, P. U. DeepAction: a MATLAB toolbox for automated classification of animal behavior in video. Sci. Rep. 13, 2688 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hu, Y. et al. LabGym: quantification of user-defined animal behaviors using learning-based holistic assessment. Cell Rep. Methods 3, 100415 (2023).

  • Marks, M. et al. Deep-learning based identification, tracking, pose estimation, and behavior classification of interacting primates and mice in complex environments. Nat. Mach. Intell. 4, 331–340 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Branson, K., Robie, A. A., Bender, J., Perona, P. & Dickinson, M. H. High-throughput ethomics in large groups of Drosophila. Nat. Methods 6, 451–457 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jia, Y. et al. Selfee, self-supervised features extraction of animal behaviors. eLife 11, e76218 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Berman, G. J., Choi, D. M., Bialek, W. & Shaevitz, J. W. Mapping the stereotyped behaviour of freely moving fruit flies. J. R. Soc. Interface 11, 20140672 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Arakawa, T. et al. Automated estimation of mouse social behaviors based on a hidden Markov model. In Hidden Markov Models: Methods and Protocols (eds Westhead, D. R. & Vijayabaskar, M. S.) 185–197 (Humana Press, 2017).

  • Chen, Z. et al. AlphaTracker: a multi-animal tracking and behavioral analysis tool. Front. Behav. Neurosci. 17, 1111908 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Huang, K. et al. A hierarchical 3D-motion learning framework for animal spontaneous behavior mapping. Nat. Commun. 12, 2784 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Luxem, K. et al. Identifying behavioral structure from deep variational embeddings of animal motion. Commun. Biol. 5, 1267 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nandi, A., Virmani, G., Barve, A. & Marathe, S. DBscorer: an open-source software for automated accurate analysis of rodent behavior in forced swim test and tail suspension test. eNeuro 8, ENEURO.0305-21.2021 (2021).

  • Gabriel, C. J. et al. BehaviorDEPOT is a simple, flexible tool for automated behavioral detection based on markerless pose tracking. eLife 11, e74314 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Golden, S. A. et al. Epigenetic regulation of RAC1 induces synaptic remodeling in stress disorders and depression. Nat. Med. 19, 337–344 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Burgos-Artizzu, X. P., Dollar, P., Lin D., Anderson, D. J. & Perona, P. CRIM13 (Caltech Resident-Intruder Mouse 13) (1.0). CaltechDATA. https://doi.org/10.22002/D1.1892 (2021).

  • Karashchuk, P., Tuthill, J. C. & Brunton, B. W. The DANNCE of the rats: a new toolkit for 3D tracking of animal behavior. Nat. Methods 18, 460–462 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Branson, K. APT. https://github.com/kristinbranson/APT

  • Lee, W., Fu, J., Bouwman, N., Farago, P. & Curley, J. P. Temporal microstructure of dyadic social behavior during relationship formation in mice. PLoS ONE 14, e0220596 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 



  • Source link

    Leave a Reply

    Your email address will not be published. Required fields are marked *