Increasing resolution in stress neurobiology: from single cells to complex group behaviors

References

• Allen, W. E., DeNardo, L. A., Chen, M. Z., Liu, C. D., Loh, K. M., Fenno, L. E., Ramakrishnan, C., Deisseroth, K., & Luo, L. (2017). Thirst-associated preoptic neurons encode an aversive motivational drive. Science, 357(6356), 1149–1155. https://doi.org/10.1126/science.aan6747
   PubMed Web of Science ®Google Scholar
• Anpilov, S., Shemesh, Y., Eren, N., Harony-Nicolas, H., Benjamin, A., Dine, J., Oliveira, V. E. M., Forkosh, O., Karamihalev, S., Hüttl, R.-E., Feldman, N., Berger, R., Dagan, A., Chen, G., Neumann, I. D., Wagner, S., Yizhar, O., & Chen, A. (2020). Wireless optogenetic stimulation of oxytocin neurons in a semi-natural setup dynamically elevates both pro-social and agonistic behaviors. Neuron, 107(4), 644–655.e647. https://doi.org/10.1016/j.neuron.2020.05.028
   PubMed Web of Science ®Google Scholar
• Ataallahi, M., Nejad, J. G., & Park, K. H. (2022). Selection of appropriate biomatrices for studies of chronic stress in animals: A review. Journal of Animal Science and Technology, 64(4), 621–639. https://doi.org/10.5187/jast.2022.e38
   PubMed Web of Science ®Google Scholar
• Binder, F. P., & Spoormaker, V. I. (2020). Quantifying human avoidance behavior in immersive virtual reality. Frontiers in Behavioral Neuroscience, 14, 569899. https://doi.org/10.3389/fnbeh.2020.569899
   PubMed Web of Science ®Google Scholar
• Binder, F. P., Pöhlchen, D., Zwanzger, P., & Spoormaker, V. I. (2022). Facing your fear in immersive virtual reality: Avoidance behavior in specific phobia. Frontiers in Behavioral Neuroscience, 16, 827673. https://doi.org/10.3389/fnbeh.2022.827673
   PubMed Web of Science ®Google Scholar
• Bonapersona, V., Schuler, H., Damsteegt, R., Adolfs, Y., Pasterkamp, R. J., van den Heuvel, M. P., Joëls, M., & Sarabdjitsingh, R. A. (2022). The mouse brain after foot shock in four dimensions: Temporal dynamics at a single-cell resolution. Proceedings of the National Academy of Sciences of the United States of America, 119(8), e2114002119. https://doi.org/10.1073/pnas.2114002119
   PubMed Web of Science ®Google Scholar
• Bordes, J., & Miranda, L. (2022). Automatically annotated motion tracking identifies a distinct social behavioral profile following chronic social defeat stress. BioRxiv. https://doi.org/10.1101/2022.06.23.497350
   Google Scholar
• Borm, L. E., Mossi Albiach, A., Mannens, C. C. A., Janusauskas, J., Özgün, C., Fernández-García, D., Hodge, R., Castillo, F., Hedin, C. R. H., Villablanca, E. J., et al. (2022). Scalable in situ single-cell profiling by electrophoretic capture of mrna using eel fish. Nature Biotechnology, 41(2), 222–231. https://doi.org/10.1038/s41587-022-01455-3
   PubMedGoogle Scholar
• Bredikhin, D., Kats, I., & Stegle, O. (2022). Muon: Multimodal omics analysis framework. Genome Biology, 23(1), 42. https://doi.org/10.1186/s13059-021-02577-8
   PubMed Web of Science ®Google Scholar
• Brivio, E., Lopez, J. P., & Chen, A. (2020). Sex differences: Transcriptional signatures of stress exposure in male and female brains. Genes, Brain and Behavior, 19(3), e12643.
   PubMed Web of Science ®Google Scholar
• Chung, K., Wallace, J., Kim, S. Y., Kalyanasundaram, S., Andalman, A. S., Davidson, T. J., Mirzabekov, J. J., Zalocusky, K. A., Mattis, J., Denisin, A. K., et al. (2013). Structural and molecular interrogation of intact biological systems. Nature, 497(7449), 332–337. https://doi.org/10.1038/nature12107
   PubMed Web of Science ®Google Scholar
• Cruz-Mendoza, F., Jauregui-Huerta, F., Aguilar-Delgadillo, A., García-Estrada, J., & Luquin, S. (2022). Immediate early gene c-fos in the brain: Focus on glial cells. Brain Sciences, 12(6), 687. https://doi.org/10.3390/brainsci12060687
   PubMed Web of Science ®Google Scholar
• Davis, M. T., Holmes, S. E., Pietrzak, R. H., & Esterlis, I. (2017). Neurobiology of chronic stress-related psychiatric disorders: Evidence from molecular imaging studies. Chronic Stress, 1, https://doi.org/10.1177/2470547017710916
   Google Scholar
• Davoudian, P. A., Shao, L. X., & Kwan, A. C. (2023). Shared and distinct brain regions targeted for immediate early gene expression by ketamine and psilocybin. ACS Chemical Neuroscience, 14(3), 468–480. https://doi.org/10.1021/acschemneuro.2c00637
   PubMedGoogle Scholar
• de Chaumont, F., Coura, R. D., Serreau, P., Cressant, A., Chabout, J., Granon, S., & Olivo-Marin, J. C. (2012). Computerized video analysis of social interactions in mice. Nature Methods, 9(4), 410–417. https://doi.org/10.1038/nmeth.1924
   PubMed Web of Science ®Google Scholar
• Dedic, N., Chen, A., & Deussing, J. M. (2018). The crf family of neuropeptides and their receptors - mediators of the central stress response. Curr Mol Pharmacol, 11(1), 4–31.
   PubMed Web of Science ®Google Scholar
• Deffieux, T., Demené, C., & Tanter, M. (2021). Functional ultrasound imaging: A new imaging modality for neuroscience. Neuroscience, 474, 110–121. https://doi.org/10.1016/j.neuroscience.2021.03.005
   PubMed Web of Science ®Google Scholar
• Deussing, J. M., & Chen, A. (2018). The corticotropin-releasing factor family: Physiology of the stress response. Physiological Reviews, 98(4), 2225–2286. https://doi.org/10.1152/physrev.00042.2017
   PubMed Web of Science ®Google Scholar
• Dournes, C., Chen, A., & PrDournes, V. O. (2020). Hypothalamic glucocorticoid receptor in crf neurons is essential for hpa axis habituation to repeated stressor. BioRxiv,
   Google Scholar
• Engelhardt, C., Tang, F., Elkhateib, R., Bordes, J., Brix, L. M., van Doeselaar, L., Häusl, A. S., Pöhlmann, M. L., Schraut, K., Yang, H., et al. (2021). Fkbp51 in the oval bed nucleus of the stria terminalis regulates anxiety-like behavior. eNeuro, 8(6), ENEURO.0425-21.2021. https://doi.org/10.1523/ENEURO.0425-21.2021
   Google Scholar
• Feng, J., Zhang, C., Lischinsky, J. E., Jing, M., Zhou, J., Wang, H., Zhang, Y., Dong, A., Wu, Z., Wu, H., Chen, W., Zhang, P., Zou, J., Hires, S. A., Zhu, J. J., Cui, G., Lin, D., Du, J., & Li, Y. (2019). A genetically encoded fluorescent sensor for rapid and specific in vivo detection of norepinephrine. Neuron, 102(4), 745–761.e748. https://doi.org/10.1016/j.neuron.2019.02.037
   PubMed Web of Science ®Google Scholar
• Fischer, D. S., Dony, L., König, M., Moeed, A., Zappia, L., Heumos, L., Tritschler, S., Holmberg, O., Aliee, H., & Theis, F. J. (2021). Sfaira accelerates data and model reuse in single cell genomics. Genome Biology, 22(1), 248. https://doi.org/10.1186/s13059-021-02452-6
   PubMed Web of Science ®Google Scholar
• Forkosh, O., Karamihalev, S., Roeh, S., Alon, U., Anpilov, S., Touma, C., Nussbaumer, M., Flachskamm, C., Kaplick, P. M., Shemesh, Y., & Chen, A. (2019). Identity domains capture individual differences from across the behavioral repertoire. Nature Neuroscience, 22(12), 2023–2028. https://doi.org/10.1038/s41593-019-0516-y
   PubMed Web of Science ®Google Scholar
• Franceschini, A., Costantini, I., Pavone, F. S., & Silvestri, L. (2020). Dissecting neuronal activation on a brain-wide scale with immediate early genes. Frontiers in Neuroscience, 14, 569517. https://doi.org/10.3389/fnins.2020.569517
   PubMed Web of Science ®Google Scholar
• Goodwin, N. L., Nilsson, S. R. O., Choong, J. J., & Golden, S. A. (2022). Toward the explainability, transparency, and universality of machine learning for behavioral classification in neuroscience. Current Opinion in Neurobiology, 73, 102544. https://doi.org/10.1016/j.conb.2022.102544
   PubMed Web of Science ®Google Scholar
• Gururajan, A., Kos, A., & Lopez, J. P. (2018). Preclinical stress research: Where are we headed? An early career investigator’s perspective. Stress (Amsterdam, Netherlands), 21(5), 384–388. https://doi.org/10.1080/10253890.2018.1446519
   PubMed Web of Science ®Google Scholar
• Haidl, T. K., Hedderich, D. M., Rosen, M., Kaiser, N., Seves, M., Lichtenstein, T., Penzel, N., Wenzel, J., Kambeitz-Ilankovic, L., Ruef, A., Popovic, D., Schultze-Lutter, F., Chisholm, K., Upthegrove, R., Salokangas, R. K. R., Pantelis, C., Meisenzahl, E., Wood, S. J., Brambilla, P., … Koutsouleris, N. (2023). The non-specific nature of mental health and structural brain outcomes following childhood trauma. Psychological Medicine, 53(3), 1005–1014. https://doi.org/10.1017/S0033291721002439
   PubMed Web of Science ®Google Scholar
• Hamilton, P. J., Burek, D. J., Lombroso, S. I., Neve, R. L., Robison, A. J., Nestler, E. J., & Heller, E. A. (2018). Cell-type-specific epigenetic editing at the fosb gene controls susceptibility to social defeat stress. Neuropsychopharmacology: official Publication of the American College of Neuropsychopharmacology, 43(2), 272–284. https://doi.org/10.1038/npp.2017.88
   PubMed Web of Science ®Google Scholar
• Häusl, A. S., Brix, L. M., Hartmann, J., Pöhlmann, M. L., Lopez, J.-P., Menegaz, D., Brivio, E., Engelhardt, C., Roeh, S., Bajaj, T., Rudolph, L., Stoffel, R., Hafner, K., Goss, H. M., Reul, J. M. H. M., Deussing, J. M., Eder, M., Ressler, K. J., Gassen, N. C., Chen, A., & Schmidt, M. V. (2021). The co-chaperone fkbp5 shapes the acute stress response in the paraventricular nucleus of the hypothalamus of male mice. Molecular Psychiatry, 26(7), 3060–3076. https://doi.org/10.1038/s41380-021-01044-x
   PubMed Web of Science ®Google Scholar
• Hökfelt, T., Barde, S., Xu, Z. D., Kuteeva, E., Rüegg, J., Le Maitre, E., Risling, M., Kehr, J., Ihnatko, R., Theodorsson, E., et al. (2018). Neuropeptide and small transmitter coexistence: Fundamental studies and relevance to mental illness. Frontiers in Neural Circuits. 12, 106. https://doi.org/10.3389/fncir.2018.00106
   PubMed Web of Science ®Google Scholar
• Hsu, A. I., & Yttri, E. A. (2021). B-soid, an open-source unsupervised algorithm for identification and fast prediction of behaviors. Nature Communications, 12(1), 5188. https://doi.org/10.1038/s41467-021-25420-x
   PubMed Web of Science ®Google Scholar
• Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D. S., Quinn, K., Sanislow, C., & Wang, P. (2010). Research domain criteria (rdoc): Toward a new classification framework for research on mental disorders. The American Journal of Psychiatry, 167(7), 748–751. https://doi.org/10.1176/appi.ajp.2010.09091379
   PubMed Web of Science ®Google Scholar
• Issler, O., van der Zee, Y. Y., Ramakrishnan, A., Wang, J., Tan, C., Loh, Y.-H E., Purushothaman, I., Walker, D. M., Lorsch, Z. S., Hamilton, P. J., Peña, C. J., Flaherty, E., Hartley, B. J., Torres-Berrío, A., Parise, E. M., Kronman, H., Duffy, J. E., Estill, M. S., Calipari, E. S., … Nestler, E. J. (2020). Sex-specific role for the long non-coding rna linc00473 in depression. Neuron, 106(6), 912–926.e915. https://doi.org/10.1016/j.neuron.2020.03.023
   PubMed Web of Science ®Google Scholar
• Karamihalev, S., Brivio, E., Flachskamm, C., Stoffel, R., Schmidt, M. V., & Chen, A. (2020). Social dominance mediates behavioral adaptation to chronic stress in a sex-specific manner. Elife, 9, e58723. https://doi.org/10.7554/eLife.58723
   PubMed Web of Science ®Google Scholar
• Kawashima, T., Kitamura, K., Suzuki, K., Nonaka, M., Kamijo, S., Takemoto-Kimura, S., Kano, M., Okuno, H., Ohki, K., & Bito, H. (2013). Functional labeling of neurons and their projections using the synthetic activity-dependent promoter e-sare. Nature Methods, 10(9), 889–895. https://doi.org/10.1038/nmeth.2559
   PubMed Web of Science ®Google Scholar
• Kawashima, T., Okuno, H., & Bito, H. (2014). A new era for functional labeling of neurons: Activity-dependent promoters have come of age. Frontiers in Neural Circuits. 8, 37.
   PubMed Web of Science ®Google Scholar
• Koutlas, I., Linders, L. E., van der Starre, S. E., Wolterink-Donselaar, I. G., Adan, R. A. H., & Meye, F. J. (2022). Characterizing and traping a social stress-activated neuronal ensemble in the ventral tegmental area. Frontiers in Behavioral Neuroscience, 16, 936087. https://doi.org/10.3389/fnbeh.2022.936087
   PubMed Web of Science ®Google Scholar
• Koutsouleris, V. W. (2022). Neurominer [computer software]. GitHub.
   Google Scholar
• Kuti, D., Winkler, Z., Horváth, K., Juhász, B., Szilvásy-Szabó, A., Fekete, C., Ferenczi, S., & Kovács, K. J. (2022). The metabolic stress response: Adaptation to acute-, repeated- and chronic challenges in mice. iScience, 25(8), 104693. https://doi.org/10.1016/j.isci.2022.104693
   PubMed Web of Science ®Google Scholar
• Kwon, D. Y., Xu, B., Hu, P., Zhao, Y.-T., Beagan, J. A., Nofziger, J. H., Cui, Y., Phillips-Cremins, J. E., Blendy, J. A., Wu, H., & Zhou, Z. (2022). Neuronal yin yang1 in the prefrontal cortex regulates transcriptional and behavioral responses to chronic stress in mice. Nature Communications, 13(1), 55. https://doi.org/10.1038/s41467-021-27571-3
   PubMed Web of Science ®Google Scholar
• Lauer, J., Zhou, M., Ye, S., Menegas, W., Schneider, S., Nath, T., Rahman, M. M., Di Santo, V., Soberanes, D., Feng, G., Murthy, V. N., Lauder, G., Dulac, C., Mathis, M. W., & Mathis, A. (2022). Multi-animal pose estimation, identification and tracking with deeplabcut. Nature Methods, 19(4), 496–504. https://doi.org/10.1038/s41592-022-01443-0
   PubMed Web of Science ®Google Scholar
• Lin, R., Lopez, J. P., Cruceanu, C., Pierotti, C., Fiori, L. M., Squassina, A., Chillotti, C., Dieterich, C., Mellios, N., & Turecki, G. (2021). Circular rna circccnt2 is upregulated in the anterior cingulate cortex of individuals with bipolar disorder. Translational Psychiatry, 11(1), 629. https://doi.org/10.1038/s41398-021-01746-4
   PubMed Web of Science ®Google Scholar
• Lopez, J. P., Brivio, E., Santambrogio, A., De Donno, C., Kos, A., Peters, M., Rost, N., Czamara, D., Brückl, T. M., Roeh, S., et al. (2021). Single-cell molecular profiling of all three components of the hpa axis reveals adrenal abcb1 as a regulator of stress adaptation. Science Advances. 7(5), eabe4497. https://doi.org/10.1126/sciadv.abe4497
   PubMed Web of Science ®Google Scholar
• Lopez, J. P., Kos, A., & Turecki, G. (2018). Major depression and its treatment: Micrornas as peripheral biomarkers of diagnosis and treatment response. Current Opinion in Psychiatry, 31(1), 7–16. https://doi.org/10.1097/YCO.0000000000000379
   PubMed Web of Science ®Google Scholar
• Lopez, J. P., Lücken, M. D., Brivio, E., Karamihalev, S., Kos, A., De Donno, C., Benjamin, A., Yang, H., Dick, A. L. W., Stoffel, R., Flachskamm, C., Ressle, A., Roeh, S., Huettl, R.-E., Parl, A., Eggert, C., Novak, B., Yan, Y., Yeoh, K., … Chen, A. (2022). Ketamine exerts its sustained antidepressant effects via cell-type-specific regulation of kcnq2. Neuron, 110(14), 2283–2298.e2289. https://doi.org/10.1016/j.neuron.2022.05.001
   PubMed Web of Science ®Google Scholar
• Luecken, M. D., & Theis, F. J. (2019). Current best practices in single-cell rna-seq analysis: A tutorial. Molecular Systems Biology, 15(6), e8746. https://doi.org/10.15252/msb.20188746
   PubMed Web of Science ®Google Scholar
• Luutonen, S., Tikka, M., Karlsson, H., & Salokangas, R. K. (2013). Childhood trauma and distress experiences associate with psychotic symptoms in patients attending primary and psychiatric outpatient care. Results of the radep study. European Psychiatry: The Journal of the Association of European Psychiatrists, 28(3), 154–160. https://doi.org/10.1016/j.eurpsy.2011.11.005
   PubMedGoogle Scholar
• Luxem, K., Mocellin, P., Fuhrmann, F., Kürsch, J., Miller, S. R., Palop, J. J., Remy, S., & Bauer, P. (2022). Identifying behavioral structure from deep variational embeddings of animal motion. Communications Biology, 5(1), 1267. https://doi.org/10.1038/s42003-022-04080-7
   PubMed Web of Science ®Google Scholar
• Mandino, F., Cerri, D. H., Garin, C. M., Straathof, M., van Tilborg, G. A. F., Chakravarty, M. M., Dhenain, M., Dijkhuizen, R. M., Gozzi, A., Hess, A., et al. (2019). Animal functional magnetic resonance imaging: Trends and path toward standardization. Frontiers in Neuroinformatics, 13, 78.
   PubMed Web of Science ®Google Scholar
• Marks, M., Qiuhan, J., Sturman, O., von Ziegler, L., Kollmorgen, S., von der Behrens, W., Mante, V., Bohacek, J., & Yanik, M. F. (2022). Deep-learning based identification, tracking, pose estimation, and behavior classification of interacting primates and mice in complex environments. Nature Machine Intelligence, 4(4), 331–340. https://doi.org/10.1038/s42256-022-00477-5
   PubMedGoogle Scholar
• Mathis, A., Mamidanna, P., Cury, K. M., Abe, T., Murthy, V. N., Mathis, M. W., & Bethge, M. (2018). Deeplabcut: Markerless pose estimation of user-defined body parts with deep learning. Nature Neuroscience, 21(9), 1281–1289. https://doi.org/10.1038/s41593-018-0209-y
   PubMed Web of Science ®Google Scholar
• Maynard, K. R., Collado-Torres, L., Weber, L. M., Uytingco, C., Barry, B. K., Williams, S. R., Catallini, J. L., Tran, M. N., Besich, Z., Tippani, M., Chew, J., Yin, Y., Kleinman, J. E., Hyde, T. M., Rao, N., Hicks, S. C., Martinowich, K., & Jaffe, A. E. (2021). Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex. Nature Neuroscience, 24(3), 425–436. https://doi.org/10.1038/s41593-020-00787-0
   PubMed Web of Science ®Google Scholar
• Miranda, L., Paul, R., Pütz, B., Koutsouleris, N., & Müller-Myhsok, B. (2021). Systematic review of functional mri applications for psychiatric disease subtyping. Frontiers in Psychiatry, 12, 665536. https://doi.org/10.3389/fpsyt.2021.665536
   PubMed Web of Science ®Google Scholar
• Moffitt, J. R., Lundberg, E., & Heyn, H. (2022). The emerging landscape of spatial profiling technologies. Nature Reviews. Genetics, 23(12), 741–759. https://doi.org/10.1038/s41576-022-00515-3
   PubMed Web of Science ®Google Scholar
• Morris, S. E., Sanislow, C. A., Pacheco, J., Vaidyanathan, U., Gordon, J. A., & Cuthbert, B. N. (2022). Revisiting the seven pillars of rdoc. BMC Medicine, 20(1), 220. https://doi.org/10.1186/s12916-022-02414-0
   PubMed Web of Science ®Google Scholar
• Musazzi, L., & Marrocco, J. (2016). The many faces of stress: Implications for neuropsychiatric disorders. Neural Plasticity, 2016, 8389737. https://doi.org/10.1155/2016/8389737
   PubMed Web of Science ®Google Scholar
• Musazzi, L., Tornese, P., Sala, N., & Popoli, M. (2018). What acute stress protocols can tell us about ptsd and stress-related neuropsychiatric disorders. Frontiers in Pharmacology. 9, 758. https://doi.org/10.3389/fphar.2018.00758
   PubMed Web of Science ®Google Scholar
• Nilsson, S. (2022). Simple behavioral analysis (simba) – an open source toolkit for computer classification of complex social behaviors in experimental animals. BioRxiv,
   Google Scholar
• Niu, M., Kasai, A., Tanuma, M., Seiriki, K., Igarashi, H., Kuwaki, T., Nagayasu, K., Miyaji, K., Ueno, H., Tanabe, W., et al. (2022). Claustrum mediates bidirectional and reversible control of stress-induced anxiety responses. Science Advances. 8(11), eabi6375. https://doi.org/10.1126/sciadv.abi6375
   PubMed Web of Science ®Google Scholar
• Palla, G., Spitzer, H., Klein, M., Fischer, D., Schaar, A. C., Kuemmerle, L. B., Rybakov, S., Ibarra, I. L., Holmberg, O., Virshup, I., Lotfollahi, M., Richter, S., & Theis, F. J. (2022). Squidpy: A scalable framework for spatial omics analysis. Nature Methods, 19(2), 171–178. https://doi.org/10.1038/s41592-021-01358-2
   PubMed Web of Science ®Google Scholar
• 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.-H., Falkner, A. L., Shaevitz, J. W., & Murthy, M. (2022). Sleap: A deep learning system for multi-animal pose tracking. Nature Methods, 19(4), 486–495. https://doi.org/10.1038/s41592-022-01426-1
   PubMed Web of Science ®Google Scholar
• Popovic, D., Ruef, A., Dwyer, D. B., Antonucci, L. A., Eder, J., Sanfelici, R., Kambeitz-Ilankovic, L., Oztuerk, O. F., Dong, M. S., Paul, R., Paolini, M., Hedderich, D., Haidl, T., Kambeitz, J., Ruhrmann, S., Chisholm, K., Schultze-Lutter, F., Falkai, P., Pergola, G., … Koutsouleris, N, PRONIA Consortium. (2020). Traces of trauma: A multivariate pattern analysis of childhood trauma, brain structure, and clinical phenotypes. Biological Psychiatry, 88(11), 829–842. https://doi.org/10.1016/j.biopsych.2020.05.020
   PubMed Web of Science ®Google Scholar
• Ramirez, S., Liu, X., MacDonald, C. J., Moffa, A., Zhou, J., Redondo, R. L., & Tonegawa, S. (2015). Activating positive memory engrams suppresses depression-like behaviour. Nature, 522(7556), 335–339. https://doi.org/10.1038/nature14514
   PubMed Web of Science ®Google Scholar
• Renier, N., Wu, Z., Simon, D. J., Yang, J., Ariel, P., & Tessier-Lavigne, M. (2014). Idisco: A simple, rapid method to immunolabel large tissue samples for volume imaging. Cell, 159(4), 896–910. https://doi.org/10.1016/j.cell.2014.10.010
   PubMed Web of Science ®Google Scholar
• Russell, G., & Lightman, S. (2019). The human stress response. Nature Reviews. Endocrinology, 15(9), 525–534. https://doi.org/10.1038/s41574-019-0228-0
   PubMed Web of Science ®Google Scholar
• Sanacora, G., Yan, Z., & Popoli, M. (2022). The stressed synapse 2.0: Pathophysiological mechanisms in stress-related neuropsychiatric disorders. Nature Reviews. Neuroscience, 23(2), 86–103. https://doi.org/10.1038/s41583-021-00540-x
   PubMed Web of Science ®Google Scholar
• Satija, R., Farrell, J. A., Gennert, D., Schier, A. F., & Regev, A. (2015). Spatial reconstruction of single-cell gene expression data. Nature Biotechnology, 33(5), 495–502. https://doi.org/10.1038/nbt.3192
   PubMed Web of Science ®Google Scholar
• Scharf, S. H., Liebl, C., Binder, E. B., Schmidt, M. V., & Müller, M. B. (2011). Expression and regulation of the fkbp5 gene in the adult mouse brain. PloS One, 6(2), e16883. https://doi.org/10.1371/journal.pone.0016883
   PubMed Web of Science ®Google Scholar
• Schneider, S., Lee, J. H., & Mathis, M. W. (2022). Learnable latent embeddings for joint behavioral and neural analysis. ArXiv,
   Google Scholar
• Segalin, C., Williams, J., Karigo, T., Hui, M., Zelikowsky, M., Sun, J. J., Perona, P., Anderson, D. J., & Kennedy, A. (2021). The mouse action recognition system (mars) software pipeline for automated analysis of social behaviors in mice. Elife, 10, e63720. https://doi.org/10.7554/eLife.63720
   PubMed Web of Science ®Google Scholar
• Shemesh, Y., & Chen, A. (2023). A paradigm shift in translational psychiatry through rodent neuroethology. Molecular Psychiatry, 28, 993–1003. https://doi.org/10.1038/s41380-022-01913-z
   PubMed Web of Science ®Google Scholar
• Shemesh, Y., Forkosh, O., Mahn, M., Anpilov, S., Sztainberg, Y., Manashirov, S., Shlapobersky, T., Elliott, E., Tabouy, L., Ezra, G., Adler, E. S., Ben-Efraim, Y. J., Gil, S., Kuperman, Y., Haramati, S., Dine, J., Eder, M., Deussing, J. M., Schneidman, E., Yizhar, O., & Chen, A. (2016). Ucn3 and crf-r2 in the medial amygdala regulate complex social dynamics. Nature Neuroscience, 19(11), 1489–1496. https://doi.org/10.1038/nn.4346
   PubMed Web of Science ®Google Scholar
• Shemesh, Y., Sztainberg, Y., Forkosh, O., Shlapobersky, T., Chen, A., & Schneidman, E. (2013). High-order social interactions in groups of mice. eLife, 2, e00759. https://doi.org/10.7554/eLife.00759
   PubMed Web of Science ®Google Scholar
• Short, A. K. (2021). Single-cell transcriptional changes in hypothalamic corticotropin-releasing factor–expressing neurons after early-life adversity inform enduring alterations in vulnerabilities to stress (T. Z. Baram, Ed.) Biological Psychiatry Global Open Science.
   Google Scholar
• Silva, B. A., Burns, A. M., & Gräff, J. (2019). A cfos activation map of remote fear memory attenuation. Psychopharmacology, 236(1), 369–381. https://doi.org/10.1007/s00213-018-5000-y
   PubMed Web of Science ®Google Scholar
• Stahlschmidt, S. R., Ulfenborg, B., & Synnergren, J. (2022). Multimodal deep learning for biomedical data fusion: A review. Brief Bioinform, 23(2), 1–15.
   Web of Science ®Google Scholar
• Sturman, O., von Ziegler, L., Schläppi, C., Akyol, F., Privitera, M., Slominski, D., Grimm, C., Thieren, L., Zerbi, V., Grewe, B., & Bohacek, J. (2020). Deep learning-based behavioral analysis reaches human accuracy and is capable of outperforming commercial solutions. Neuropsychopharmacology: official Publication of the American College of Neuropsychopharmacology, 45(11), 1942–1952. https://doi.org/10.1038/s41386-020-0776-y
   PubMed Web of Science ®Google Scholar
• Tian, L., Chen, F., & Macosko, E. Z. (2022). The expanding vistas of spatial transcriptomics. Nature Biotechnology. https://doi.org/10.1038/s41587-022-01448-2
   Web of Science ®Google Scholar
• Tighe, P. J., Ryder, R. R., Todd, I., & Fairclough, L. C. (2015). Elisa in the multiplex era: Potentials and pitfalls. Proteomics. Clinical Applications, 9(3-4), 406–422. https://doi.org/10.1002/prca.201400130
   PubMed Web of Science ®Google Scholar
• Velten, B., Braunger, J. M., Argelaguet, R., Arnol, D., Wirbel, J., Bredikhin, D., Zeller, G., & Stegle, O. (2022). Identifying temporal and spatial patterns of variation from multimodal data using mefisto. Nature Methods, 19(2), 179–186. https://doi.org/10.1038/s41592-021-01343-9
   PubMed Web of Science ®Google Scholar
• von Mücke-Heim, I. A., Urbina-Treviño, L., Bordes, J., Ries, C., Schmidt, M. V., & Deussing, J. M. (2022). Introducing a depression-like syndrome for translational neuropsychiatry: A plea for taxonomical validity and improved comparability between humans and mice. Molecular Psychiatry. 28(1), 329–340. https://doi.org/10.1038/s41380-022-01762-w
   PubMed Web of Science ®Google Scholar
• von Ziegler, L. M., Floriou-Servou, A., Waag, R., Das Gupta, R. R., Sturman, O., Gapp, K., Maat, C. A., Kockmann, T., Lin, H.-Y., Duss, S. N., Privitera, M., Hinte, L., von Meyenn, F., Zeilhofer, H. U., Germain, P.-L., & Bohacek, J. (2022). Multiomic profiling of the acute stress response in the mouse hippocampus. Nature Communications, 13(1), 1824. https://doi.org/10.1038/s41467-022-29367-5
   PubMed Web of Science ®Google Scholar
• Wang, X.-J., Hu, H., Huang, C., Kennedy, H., Li, C. T., Logothetis, N., Lu, Z.-L., Luo, Q., Poo, M.-M., Tsao, D., Wu, S., Wu, Z., Zhang, X., & Zhou, D. (2020). Computational neuroscience: A frontier of the 21. National Science Review, 7(9), 1418–1422. https://doi.org/10.1093/nsr/nwaa129
   PubMed Web of Science ®Google Scholar
• Wen, L., Li, G., Huang, T., Geng, W., Pei, H., Yang, J., Zhu, M., Zhang, P., Hou, R., Tian, G., Su, W., Chen, J., Zhang, D., Zhu, P., Zhang, W., Zhang, X., Zhang, N., Zhao, Y., Cao, X., … Chen, Z.-J. (2022). Single-cell technologies: From research to application. Innovation (Cambridge (Mass.)), 3(6), 100342. https://doi.org/10.1016/j.xinn.2022.100342
   PubMedGoogle Scholar
• Wolf, F. A., Angerer, P., & Theis, F. J. (2018). Scanpy: Large-scale single-cell gene expression data analysis. Genome Biology, 19(1), 15. https://doi.org/10.1186/s13059-017-1382-0
   PubMed Web of Science ®Google Scholar
• Wu, Z., Lin, D., & Li, Y. (2022). Pushing the frontiers: Tools for monitoring neurotransmitters and neuromodulators. Nature Reviews. Neuroscience, 23(5), 257–274. https://doi.org/10.1038/s41583-022-00577-6
   PubMed Web of Science ®Google Scholar
• Ye, S., Mathis, A., & Mathis, M. W. (2022). Panoptic animal pose estimators are zero-shot performers. Arxiv,
   Google Scholar