Engagement of basal amygdala-nucleus accumbens glutamate neurons in the processing of rewarding or aversive social stimuli.
basal amygdala
c-Fos
calcium activity
nucleus accumbens
social aversion
social reward
Journal
The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110
Informations de publication
Date de publication:
Mar 2024
Mar 2024
Historique:
revised:
27
12
2023
received:
22
08
2023
accepted:
22
01
2024
pubmed:
8
2
2024
medline:
8
2
2024
entrez:
7
2
2024
Statut:
ppublish
Résumé
Basal amygdala (BA) neurons projecting to nucleus accumbens (NAc) core/shell are primarily glutamatergic and are integral to the circuitry of emotional processing. Several recent mouse studies have addressed whether neurons in this population(s) respond to reward, aversion or both emotional valences. The focus has been on processing of physical emotional stimuli, and here, we extend this to salient social stimuli. In male mice, an iterative study was conducted into engagement of BA-NAc neurons in response to estrous female (social reward, SR) and/or aggressive-dominant male (social aversion, SA). In BL/6J mice, SR and SA activated c-Fos expression in a high and similar number/density of BA-NAc neurons in the anteroposterior intermediate BA (int-BA), whereas activation was predominantly by SA in posterior (post-)BA. In Fos-TRAP2 mice, compared with SR-SR or SA-SA controls, exposure to successive presentation of SR-SA or SA-SR, followed by assessment of tdTomato reporter and/or c-Fos expression, demonstrated that many int-BA-NAc neurons were activated by only one of SR and SA; these SR/SA monovalent neurons were similar in number and present in both magnocellular and parvocellular int-BA subregions. In freely moving BL/6J mice exposed to SR, bulk GCaMP6 fibre photometry provided confirmatory in vivo evidence for engagement of int-BA-NAc neurons during social and sexual interactions. Therefore, populations of BA-NAc glutamate neurons are engaged by salient rewarding and aversive social stimuli in a topographic and valence-specific manner; this novel evidence is important to the overall understanding of the roles of this pathway in the circuitry of socio-emotional processing.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
996-1015Subventions
Organisme : Swiss National Science Foundation
ID : 31003A_179381
Pays : Switzerland
Informations de copyright
© 2024 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
Références
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, 1149-1155. https://doi.org/10.1126/science.aan6747
Ambroggi, F., Ishikawa, A., Fields, H. L., & Nicola, S. M. (2008). Basolateral amygdala neurons facilitate reward-seeking behavior by exciting nucleus Accumbens neurons. Neuron, 59, 648-661. https://doi.org/10.1016/j.neuron.2008.07.004
Amir, A., Headley, D. B., Lee, S. C., Haufler, D., & Paré, D. (2018). Vigilance-associated gamma oscillations coordinate the ensemble activity of basolateral amygdala neurons. Neuron, 97, 656-669.e7. https://doi.org/10.1016/j.neuron.2017.12.035
Baxter, M. G., & Murray, E. A. (2002). The amygdala and reward. Nature Reviews. Neuroscience, 3, 563-573. https://doi.org/10.1038/nrn875
Belova, M. A., Paton, J. J., Morrison, S. E., & Salzman, C. D. (2007). Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala. Neuron, 55, 970-984. https://doi.org/10.1016/j.neuron.2007.08.004
Berridge, K. C. (2019). Affective valence in the brain: Modules or modes? Nature Reviews. Neuroscience, 20, 225-234. https://doi.org/10.1038/s41583-019-0122-8
Beyeler, A., Chang, C.-J., Silvestre, M., Lévêque, C., Namburi, P., Wildes, C. P., & Tye, K. M. (2018). Organization of Valence-Encoding and Projection-Defined Neurons in the basolateral amygdala. Cell Reports, 22, 905-918. https://doi.org/10.1016/j.celrep.2017.12.097
Beyeler, A., Namburi, P., Glober, G. F., Simonnet, C., Calhoon, G. G., Conyers, G. F., Luck, R., Wildes, C. P., & Tye, K. M. (2016). Divergent routing of positive and negative information from the amygdala during memory retrieval. Neuron, 90, 348-361. https://doi.org/10.1016/j.neuron.2016.03.004
Burgos-Robles, A., Kimchi, E. Y., Izadmehr, E. M., Porzenheim, M. J., Ramos-Guasp, W. A., Nieh, E. H., Felix-Ortiz, A. C., Namburi, P., Leppla, C. A., Presbrey, K. N., Anandalingam, K. K., Pagan-Rivera, P. A., Anahtar, M., Beyeler, A., & Tye, K. M. (2017). Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment. Nature Neuroscience, 20, 824-835. https://doi.org/10.1038/nn.4553
DeNardo, L. A., Liu, C. D., Allen, W. E., Adams, E. L., Friedmann, D., Fu, L., Guenthner, C. J., Tessier-Lavigne, M., & Luo, L. (2019). Temporal evolution of cortical ensembles promoting remote memory retrieval. Nature Neuroscience, 22, 460-469. https://doi.org/10.1038/s41593-018-0318-7
Duvarci, S., & Pare, D. (2014). Amygdala microcircuits controlling learned fear. Neuron, 82, 966-980. https://doi.org/10.1016/j.neuron.2014.04.042
Ekambaram, G., Sampath Kumar, S. K., & Joseph, L. D. (2017). Comparative study on the estimation of estrous cycle in mice by visual and vaginal lavage method. Journal of Clinical and Diagnostic Research, 11, AC05-AC07. https://doi.org/10.7860/JCDR/2017/23977.9148
Franklin, K., & Paxinos, G. (2019). The mouse brain in stereotaxic coordinates (V. ed.). Elsevier.
Gore, F., Schwartz, E. C., Brangers, B. C., Aladi, S., Stujenske, J. M., Likhtik, E., Russo, M. J., Gordon, J. A., Salzman, C. D., & Axel, R. (2015). Neural representations of unconditioned stimuli in basolateral amygdala mediate innate and learned responses. Cell, 162, 134-145. https://doi.org/10.1016/j.cell.2015.06.027
Grewe, B. F., Gründemann, J., Kitch, L. J., Lecoq, J. A., Parker, J. G., Marshall, J. D., Larkin, M. C., Jercog, P. E., Grenier, F., Li, J. Z., Lüthi, A., & Schnitzer, M. J. (2017). Neural ensemble dynamics underlying a long-term associative memory. Nature, 543, 670-675. https://doi.org/10.1038/nature21682
Griffin, J. M., Fuhrer, R., Stansfeld, S. A., & Marmot, M. (2002). The importance of low control at work and home on depression and anxiety: Do these effects vary by gender and social class? Social Science & Medicine, 54, 783-798. https://doi.org/10.1016/S0277-9536(01)00109-5
Guenthner, C. J., Miyamichi, K., Yang, H. H., Heller, H. C., & Luo, L. (2013). Permanent genetic access to transiently active neurons via TRAP: Targeted recombination in active populations. Neuron, 78, 773-784. https://doi.org/10.1016/j.neuron.2013.03.025
Gururajan, A., Reif, A., Cryan, J. F., & Slattery, D. A. (2019). The future of rodent models in depression research. Nature Reviews. Neuroscience, 20, 686-701. https://doi.org/10.1038/s41583-019-0221-6
Ineichen, C., Greter, A., Baer, M., Sigrist, H., Sautter, E., Sych, Y., Helmchen, F., & Pryce, C. R. (2022). Basomedial amygdala activity in mice reflects specific and general aversion uncontrollability. European Journal of Neuroscience, 55, 2435-2454. https://doi.org/10.1111/ejn.15090
Janitzky, K., D׳Hanis, W., Kröber, A., & Schwegler, H. (2015). TMT predator odor activated neural circuit in C57BL/6J mice indicates TMT-stress as a suitable model for uncontrollable intense stress. Brain Research, 1599, 1-8. https://doi.org/10.1016/j.brainres.2014.12.030
Johansen, J. P., Cain, C. K., Ostroff, L. E., & Ledoux, J. E. (2011). Molecular mechanisms of fear learning and memory. Cell, 147, 509-524. https://doi.org/10.1016/j.cell.2011.10.009
Jones, J. L., Day, J. J., Aragona, B. J., Wheeler, R. A., Wightman, R. M., & Carelli, R. M. (2010). Basolateral amygdala modulates terminal dopamine release in the nucleus Accumbens and conditioned responding. Biological Psychiatry, 67, 737-744. https://doi.org/10.1016/j.biopsych.2009.11.006
Kim, J., Pignatelli, M., Xu, S., Itohara, S., & Tonegawa, S. (2016). Antagonistic negative and positive neurons of the basolateral amygdala. Nature Neuroscience, 19, 1636-1646. https://doi.org/10.1038/nn.4414
Kirschbaum, C., Pirke, K.-M., & Hellhammer, D. H. (2004). The ‘Trier social stress test’ - A tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology, 28, 76-81. https://doi.org/10.1159/000119004
Kyriazi, P., Headley, D. B., & Pare, D. (2018). Multi-dimensional coding by basolateral amygdala neurons. Neuron, 99, 1315-1328.e5. https://doi.org/10.1016/j.neuron.2018.07.036
Lüthi, A., & Lüscher, C. (2014). Pathological circuit function underlying addiction and anxiety disorders. Nature Neuroscience, 17, 1635-1643. https://doi.org/10.1038/nn.3849
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., Lein, E. S., & Zeng, H. (2010). A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nature Neuroscience, 13, 133-140. https://doi.org/10.1038/nn.2467
Madur, L., Ineichen, C., Bergamini, G., Greter, A., Poggi, G., Cuomo-Haymour, N., Sigrist, H., Sych, Y., Paterna, J.-C., Bornemann, K. D., Viollet, C., Fernandez-Albert, F., Alanis-Lobato, G., Hengerer, B., & Pryce, C. R. (2023). Stress deficits in reward behaviour are associated with and replicated by dysregulated amygdala-nucleus accumbens pathway function in mice. Communications Biology, 6, 422. https://doi.org/10.1038/s42003-023-04811-4
McEwen, B. S. (2007). Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiological Reviews, 87, 873-904. https://doi.org/10.1152/physrev.00041.2006
Namburi, P., Beyeler, A., Yorozu, S., Calhoon, G. G., Halbert, S. A., Wichmann, R., Holden, S. S., Mertens, K. L., Anahtar, M., Felix-Ortiz, A. C., Wickersham, I. R., Gray, J. M., & Tye, K. M. (2015). A circuit mechanism for differentiating positive and negative associations. Nature, 520, 675-678. https://doi.org/10.1038/nature14366
Pérez-Gómez, A., Bleymehl, K., Stein, B., Pyrski, M., Birnbaumer, L., Munger, S. D., Leinders-Zufall, T., Zufall, F., & Chamero, P. (2015). Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus. Current Biology, 25, 1340-1346. https://doi.org/10.1016/j.cub.2015.03.026
Pitkänen, A., Savander, V., & LeDoux, J. E. (1997). Organization of intra-amygdaloid circuitries in the rat: An emerging framework for understanding functions of the amygdala. Trends in Neurosciences, 20, 517-523. https://doi.org/10.1016/S0166-2236(97)01125-9
Pryce, C. R., & Fuchs, E. (2017). Chronic psychosocial stressors in adulthood: Studies in mice, rats and tree shrews. Neurobiol Stress, 6, 94-103. https://doi.org/10.1016/j.ynstr.2016.10.001
Rosen, J. B., Asok, A., & Chakraborty, T. (2015). The smell of fear: Innate threat of 2,5-dihydro-2,4,5-trimethylthiazoline, a single molecule component of a predator odor. Frontiers in Neuroscience, 9, 292. https://doi.org/10.3389/fnins.2015.00292
Sanders, K. M., Sakai, K., Henry, T. D., Hashimoto, T., & Akiyama, T. (2019). A subpopulation of amygdala neurons mediates the affective component of itch. Journal of Neuroscience, 39, 3345-3356. https://doi.org/10.1523/JNEUROSCI.2759-18.2019
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., & Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9, 676-682. https://doi.org/10.1038/nmeth.2019
Sesack, S. R., & Grace, A. A. (2010). Cortico-basal ganglia reward network: Microcircuitry. Neuropsychopharmacology, 35, 27-47. https://doi.org/10.1038/npp.2009.93
Zhang, X., Guan, W., Yang, T., Furlan, A., Xiao, X., Yu, K., An, X., Galbavy, W., Ramakrishnan, C., Deisseroth, K., Ritola, K., Hantman, A., He, M., Josh Huang, Z., & Li, B. (2021). Genetically identified amygdala-striatal circuits for valence-specific behaviors. Nature Neuroscience, 24, 1586-1600. https://doi.org/10.1038/s41593-021-00927-0