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Weinreb, C., Pearl, J.E., Lin, S., Osman, M.A.M., Zhang, L., Annapragada, S., Conlin, E., Hoffmann, R., Makowska, S., Gillis, W.F., Jay, M., Ye, S., Mathis, A., Mathis, M.W., Pereira, T., Linderman, S.W., Datta, S.R. Keypoint-MoSeq: parsing behavior by linking point tracking to pose dynamics. (2024) Nature Methods. 21(7):1329-1339. DOI: 10.1038/s41592-024-02318-2

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Berrigan, E.M., Wang, L., Carrillo, H., Echegoyen, K., Kappes, M., Torres, J., Ai-Perreira, A., McCoy, E., Shane, E., Copeland, C.D., Ragel, L., Georgousakis, C., Lee, S., Reynolds, D., Talgo, A., Gonzalez, J., Zhang, L., Rajurkar, A.B., Ruiz, M., Daniels, E., Maree, L., Pariyar, S., Busch, W., Pereira, T.D. Fast and Efficient Root Phenotyping via Pose Estimation. (2024) Plant Phenomics. 6:0175. DOI: 10.34133/plantphenomics.0175

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Mitelut, C., Diez Castro, M., Peterson, R.E., Goncalves, M., Li, J., Gamer, M.M., Nilsson, S.R.O., Pereira, T.D., Sanes, D.H. A behavioral roadmap for the development of agency in the rodent. (2024) bioRxiv. DOI: 10.1101/2023.11.10.566632

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Tye, K., Patel, R., Patarino, M., Kim, K., Pamintuan, R., Taschbach, F., Li, H., Lee, C., Hoek, A., Castro, R., Cazares, C., Miranda, R., Jia, C., Delahanty, J., Batra, K., Keyes, L., Libster, A., Wichmann, R., Pereira, T., Benna, M. Social isolation recruits amygdala-cortical circuitry to escalate alcohol drinking. [Preprint] (2024) Res Sq. DOI: 10.21203/rs.3.rs-4033115/v1

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Mitelut , C., Diez Castro, M., Peterson, R.E., Gonçalves , M., Gamer, M.M., Nilsson, S.R.O., Pereira, T.D., Sanes, D.H. Distinct developmental trajectories of autonomous behaviors and agency in rodents (2023) bioRxiv. DOI: https://doi.org/10.1101/2023.11.10.566632

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Luxem, K., Sun, J.J., Bradley, S.P., Krishnan, K., Yttri, E., Zimmermann, J., Pereira, T.D., Laubach, M. Open-source tools for behavioral video analysis: Setup, methods, and best practices. (2023) Elife. 12. DOI: 10.7554/eLife.79305

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Weinreb, C., Osman, M.A.M., Zhang, L., Lin, S., Pearl, J., Annapragada, S., Conlin, E., Gillis, W.F., Jay, M., Ye, S., Mathis, A., Mathis, M.W., Pereira, T., Linderman, S.W., Datta, S.R. Preprint - Keypoint-MoSeq: parsing behavior by linking point tracking to pose dynamics. (2023) bioRxiv. DOI: 10.1101/2023.03.16.532307

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Prasad, A., Manor, U., Pereira, T. Exploring the role of image domain in self-supervised DNN models of rodent brains (2022) OpenReview.net.

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Mills, F., Lee, C.R., Howe, J.R., Li, Shao, Keisler, M.N., Lemieux , M.E., Taschbach , F.H., Keyes, L.R., Borio, M., Chen, H.S., Patel, R.R., Gross, A.l., Delahanty , J., Cazares, C., Maree, L., Wichmann , R., Pereira , T.D., Benna, M.K., Root, C.M., Tye, K.M. Amygdalostriatal transition zone neurons encode sustained valence to direct conditioned behaviors (2022) bioRxiv. DOI: https://doi.org/10.1101/2022.10.28.514263

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In order to respond appropriately to threats in the environment, the brain must rapidly determine whether a stimulus is important and whether it is positive or negative, and then use that information to direct behavioral responses. Neurons in the amygdala have long been implicated in valence encoding and in fear responses to threatening stimuli, but show transient firing responses in response to these stimuli that do not match the timescales of associated behavioral responses. For decades, there has been a logical gap in how behavioral responses could be mediated without an ensemble representation of the internal state of valence that has rapid onset, high signal-to-noise, and is sustained for the duration of the behavioral state. Here, we present the amygdalostriatal transition zone (ASt) as a missing piece of this highly conserved process that is of paramount importance for survival, which does exactly this: represents an internal state (e.g. fear) that can be expressed in multiple motor outputs (e.g. freezing or escape). The ASt is anatomically positioned as a “shortcut” to connect the corticolimbic system (important for evaluation) with the basal ganglia (important for action selection) with the inputs of the amygdala and the outputs of the striatum – ideally poised for evaluating and responding to environmental threats. From in vivo cellular resolution recordings that include both electrophysiology and calcium imaging, we find that ASt neurons are unique in that they are sparse coding, extremely high signal-to-noise, and also maintain a sustained response for negative valence stimuli for the duration of the defensive behavior – a rare but essential combination. We further show that photostimulation of the ASt is sufficient to drive freezing and avoidance behaviors. Using single-nucleus RNA sequencing and in situ RNA labelling we generate a comprehensive profile of cell types and gene expression in the ASt, and find the ASt is genetically distinct from adjacent striatal and amygdalar structures. We also find that the ASt has a greater proportion of neurons expressing Drd2 than neurons expressing Drd1a, a unique feature compared to other regions of the striatum. Using in vivo calcium imaging, we show that that this Drd2+ population robustly encodes stimuli of negative valence, and in loss-of-function experiments find that optogenetic inhibition of Drd2+ ASt neurons causes a striking reduction in cue-conditioned fear responses. Together, our findings identify the ASt as a previously-unappreciated critical missing link for encoding learned associations and directing ongoing behavior.

Wang, Z.Y., McKenzie-Smith, G.C., Liu, W., Cho, H.J., Pereira, T., Dhanerawala, Z., Shaevitz, J.W., Kocher, S.D. Isolation disrupts social interactions and destabilizes brain development in bumblebees. (2022) Current Biology. DOI: 10.1016/j.cub.2022.04.066

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Pereira, T.D., Tabris, N., Matsliah, A., Turner, D.M., Li, J., Ravindranath, S., Papadoyannis, E.S., Normand, E., Deutsch, D.S., Wang, Z.Y., McKenzie-Smith, G.C., Mitelut, C.C., Castro, M.D., D'Uva, J., Kislin, M., Sanes, D.H., Kocher, S.D., Wang, S.S., Falkner, A.L., Shaevitz, J.W., Murthy, M. SLEAP: A deep learning system for multi-animal pose tracking. (2022) Nature Methods. 19(4):486-495. DOI: 10.1038/s41592-022-01426-1

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Gall, G.E.C., Pereira, T.D., Jordan, A., Meroz, Y. Fast estimation of plant growth dynamics using deep neural networks. (2022) Plant Methods. 18(1):21. DOI: 10.1186/s13007-022-00851-9

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Pereira, T.D., Shaevitz, J.W., Murthy, M. Quantifying behavior to understand the brain. (2020) Nature Neuroscience. 23(12):1537-1549. DOI: 10.1038/s41593-020-00734-z

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Deutsch, D., Pacheco, D., Encarnacion-Rivera, L., Pereira, T., Fathy, R., Clemens, J., Girardin, C., Calhoun, A., Ireland, E., Burke, A., Dorkenwald, S., McKellar, C., Macrina, T., Lu, R., Lee, K., Kemnitz, N., Ih, D., Castro, M., Halageri, A., Jordan, C., Silversmith, W., Wu, J., Seung, H.S., Murthy, M. The neural basis for a persistent internal state in females. (2020) Elife. 9. DOI: 10.7554/eLife.59502

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Jones, J.M., Foster, W., Twomey, C.R., Burdge, J., Ahmed, O.M., Pereira, T.D., Wojick, J.A., Corder, G., Plotkin, J.B., Abdus-Saboor, I. A machine-vision approach for automated pain measurement at millisecond timescales. (2020) Elife. 9. DOI: 10.7554/eLife.57258

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Charles, A.S., Falk, B., Turner, N., Pereira, T.D., Tward, D., Pedigo, B.D., Chung, J., Burns, R., Ghosh, S.S., Kebschull, J.M., Silversmith, W., Vogelstein, J.T. Toward Community-Driven Big Open Brain Science: Open Big Data and Tools for Structure, Function, and Genetics. (2020) Annual Review of Neuroscience. 43:441-464. DOI: 10.1146/annurev-neuro-100119-110036

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Pereira, T.D., Aldarondo, D.E., Willmore, L., Kislin, M., Wang, S.S., Murthy, M., Shaevitz, J.W. Fast animal pose estimation using deep neural networks. (2019) Nature Methods. 16(1):117-125. DOI: 10.1038/s41592-018-0234-5

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Badura, A., Verpeut, J.L., Metzger, J.W., Pereira, T.D., Pisano, T.J., Deverett, B., Bakshinskaya, D.E., Wang, S.S. Normal cognitive and social development require posterior cerebellar activity. (2018) Elife. 7. DOI: 10.7554/eLife.36401

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Clemens, J., Coen, P., Roemschied, F.A., Pereira, T.D., Mazumder, D., Aldarondo, D.E., Pacheco, D.A., Murthy, M. Discovery of a New Song Mode in Drosophila Reveals Hidden Structure in the Sensory and Neural Drivers of Behavior. (2018) Current Biology. 28(15):2400-2412.e6. DOI: 10.1016/j.cub.2018.06.011

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Pereira, T.D., Murthy, M. To Fight or Not to Fight. (2017) Neuron. 95(5):986-988. DOI: 10.1016/j.neuron.2017.08.029

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Giovannucci, A., Badura, A., Deverett, B., Najafi, F., Pereira, T.D., Gao, Z., Ozden, I., Kloth, A.D., Pnevmatikakis, E., Paninski, L., De Zeeuw, C.I., Medina, J.F., Wang, S.S. Cerebellar granule cells acquire a widespread predictive feedback signal during motor learning. (2017) Nature Neuroscience. 20(5):727-734. DOI: 10.1038/nn.4531

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Hobbs, E.T., Pereira, T., O'Neill, P.K., Erill, I. A Bayesian inference method for the analysis of transcriptional regulatory networks in metagenomic data. (2016) Algorithms Mol Biol. 11:19. DOI: 10.1186/s13015-016-0082-8

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Talmo Pereira, PhD

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