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Stress
The International Journal on the Biology of Stress
Volume 27, 2024 - Issue 1
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Research Article

Inhibition of prefrontal cortex parvalbumin interneurons mitigates behavioral and physiological sequelae of chronic stress in male mice

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Article: 2361238 | Received 26 May 2023, Accepted 22 May 2024, Published online: 04 Jul 2024

References

  • Ahrens, S., Wu, M. V., Furlan, A., Hwang, G. R., Paik, R., Li, H., Penzo, M. A., Tollkuhn, J., & Li, B. (2018). A central extended amygdala circuit that modulates anxiety. The Journal of Neuroscience, 38(24), 1–14. https://doi.org/10.1523/JNEUROSCI.0705-18.2018
  • Bedse, G., Hartley, N. D., Neale, E., Gaulden, A. D., Patrick, T. A., Kingsley, P. J., Uddin, M. J., Plath, N., Marnett, L. J., & Patel, S. (2017). Functional redundancy between canonical endocannabinoid signaling systems in the modulation of anxiety. Biological Psychiatry, 82(7), 488–499. https://doi.org/10.1016/j.biopsych.2017.03.002
  • Bhutada, P., Mundhada, Y., Bansod, K., Ubgade, A., Quazi, M., Umathe, S., & Mundhada, D. (2010). Reversal by quercetin of corticotrophin releasing factor induced anxiety- and depression-like effect in mice. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 34(6), 955–960. https://doi.org/10.1016/j.pnpbp.2010.04.025
  • Can, A., Dao, D. T., Terrillion, C. E., Piantadosi, S. C., Bhat, S., & Gould, T. D. (2012). The tail suspension test. Jove- Journal of Visualized Experiments, 29, e3638.
  • Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L. H., & Moore, C. I. (2009). Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature, 459(7247), 663–667. https://doi.org/10.1038/nature08002
  • Courtin, J., Chaudun, F., Rozeske, R. R., Karalis, N., Gonzalez-Campo, C., Wurtz, H., Abdi, A., Baufreton, J., Bienvenu, T. C., & Herry, C. (2014). Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature, 505(7481), 92–96. https://doi.org/10.1038/nature12755
  • Duman, R. S. (2014). Pathophysiology of depression and innovative treatments: Remodeling glutamatergic synaptic connections. Dialogues in Clinical Neuroscience, 16(1), 11–27. https://doi.org/10.31887/DCNS.2014.16.1/rduman
  • Engin, E., Smith, K. S., Gao, Y., Nagy, D., Foster, R. A., Tsvetkov, E., Keist, R., Crestani, F., Fritschy, J. M., Bolshakov, V. Y., Hajos, M., Heldt, S. A., & Rudolph, U. (2016). Modulation of anxiety and fear via distinct intrahippocampal circuits. eLife, 5, e14120. https://doi.org/10.7554/eLife.14120
  • Ferguson, B. R., & Gao, W. J. (2018). PV interneurons: Critical regulators of E/I balance for prefrontal cortex-dependent behavior and psychiatric disorders. Frontiers in Neural Circuits, 12, 37. https://doi.org/10.3389/fncir.2018.00037
  • Flak, J. N., Solomon, M. B., Jankord, R., Krause, E. G., & Herman, J. P. (2012). Identification of chronic stress-activated regions reveals a potential recruited circuit in rat brain. The European Journal of Neuroscience, 36(4), 2547–2555. https://doi.org/10.1111/j.1460-9568.2012.08161.x
  • Fogaça, M. V., Wu, M., Li, C., Li, X. Y., Picciotto, M. R., & Duman, R. S. (2021). Inhibition of GABA interneurons in the mPFC is sufficient and necessary for rapid antidepressant responses. Molecular Psychiatry, 26(7), 3277–3291. https://doi.org/10.1038/s41380-020-00916-y
  • Ghosal, S., Hare, B., & Duman, R. S. (2017). Prefrontal cortex GABAergic deficits and circuit dysfunction in the pathophysiology and treatment of chronic stress and depression. Current Opinion in Behavioral Sciences, 14, 1–8. https://doi.org/10.1016/j.cobeha.2016.09.012
  • Ghosal, S., Packard, A. E. B., Mahbod, P., McKlveen, J. M., Seeley, R. J., Myers, B., Ulrich-Lai, Y., Smith, E. P., D’Alessio, D. A., & Herman, J. P. (2017). Disruption of glucagon-like peptide 1 signaling in sim1 neurons reduces physiological and behavioral reactivity to acute and chronic stress. Journal of Neuroscience, 37, 184–193.
  • Guilloux, J. P., Seney, M., Edgar, N., & Sibille, E. (2011). Integrated behavioral z-scoring increases the sensitivity and reliability of behavioral phenotyping in mice: Relevance to emotionality and sex. Journal of Neuroscience Methods, 197(1), 21–31. https://doi.org/10.1016/j.jneumeth.2011.01.019
  • Hasler, G., van der Veen, J. W., Tumonis, T., Meyers, N., Shen, J., & Drevets, W. C. (2007). Reduced prefrontal glutamate/glutamine and gamma-aminobutyric acid levels in major depression determined using proton magnetic resonance spectroscopy. Archives of General Psychiatry, 64(2), 193–200. https://doi.org/10.1001/archpsyc.64.2.193
  • Herman, J. P. (2013). Neural control of chronic stress adaptation. Frontiers in Behavioral Neuroscience, 7, 61. https://doi.org/10.3389/fnbeh.2013.00061
  • Herman, J. P., Ostrander, M. M., Mueller, N. K., & Figueiredo, H. (2005). Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 29(8), 1201–1213. https://doi.org/10.1016/j.pnpbp.2005.08.006
  • Khan, A., de Jong, L. A., Kamenski, M. E., Higa, K. K., Lucero, J. D., Young, J. W., Behrens, M. M., & Powell, S. B. (2017). Adolescent GBR12909 exposure induces oxidative stress, disrupts parvalbumin-positive interneurons, and leads to hyperactivity and impulsivity in adult mice. Neuroscience, 345, 166–175. https://doi.org/10.1016/j.neuroscience.2016.11.022
  • Liu, M. Y., Yin, C. Y., Zhu, L. J., Zhu, X. H., Xu, C., Luo, C. X., Chen, H., Zhu, D. Y., & Zhou, Q. G. (2018). Sucrose preference test for measurement of stress-induced anhedonia in mice. Nature Protocols, 13(7), 1686–1698. https://doi.org/10.1038/s41596-018-0011-z
  • Lueptow, L. M. (2017). Novel object recognition test for the investigation of learning and memory in mice. Journal of Visualized Experiments: JoVE, 126, 55718
  • Luscher, B., Shen, Q., & Sahir, N. (2011). The GABAergic deficit hypothesis of major depressive disorder. Molecular Psychiatry, 16(4), 383–406. https://doi.org/10.1038/mp.2010.120
  • McKlveen, J. M., Moloney, R. D., Scheimann, J. R., Myers, B., & Herman, J. P. (2019). "Braking" the prefrontal cortex: The role of glucocorticoids and interneurons in stress adaptation and pathology. Biological Psychiatry, 86(9), 669–681. https://doi.org/10.1016/j.biopsych.2019.04.032
  • McKlveen, J. M., Morano, R. L., Fitzgerald, M., Zoubovsky, S., Cassella, S. N., Scheimann, J. R., Ghosal, S., Mahbod, P., Packard, B. A., Myers, B., Baccei, M. L., & Herman, J. P. (2016). Chronic stress increases prefrontal inhibition: A mechanism for stress-induced prefrontal dysfunction. Biological Psychiatry, 80(10), 754–764. https://doi.org/10.1016/j.biopsych.2016.03.2101
  • Mehta, V., Parashar, A., & Udayabanu, M. (2017). Quercetin prevents chronic unpredictable stress induced behavioral dysfunction in mice by alleviating hippocampal oxidative and inflammatory stress. Physiology & Behavior, 171, 69–78. https://doi.org/10.1016/j.physbeh.2017.01.006
  • Mourlon, V., Baudin, A., Blanc, O., Lauber, A., Giros, B., Naudon, L., & Daugé, V. (2010). Maternal deprivation induces depressive-like behaviours only in female rats. Behavioural Brain Research, 213(2), 278–287. https://doi.org/10.1016/j.bbr.2010.05.017
  • Mukherjee, A., & Caroni, P. (2018). Infralimbic cortex is required for learning alternatives to prelimbic promoted associations through reciprocal connectivity. Nature Communications, 9(1), 2727. https://doi.org/10.1038/s41467-018-05318-x
  • Nawreen, N., Cotella, E. M., Morano, R., Mahbod, P., Dalal, K. S., Fitzgerald, M., Martelle, S., Packard, B. A., Franco-Villanueva, A., Moloney, R. D., & Herman, J. P. (2020). Chemogenetic inhibition of infralimbic prefrontal cortex GABAergic parvalbumin interneurons attenuates the impact of chronic stress in male mice. eNeuro, 7(5), ENEURO.0423-19.2020. https://doi.org/10.1523/ENEURO.0423-19.2020
  • Ohira, K., Takeuchi, R., Iwanaga, T., & Miyakawa, T. (2013). Chronic fluoxetine treatment reduces parvalbumin expression and perineuronal nets in gamma-aminobutyric acidergic interneurons of the frontal cortex in adult mice. Molecular Brain, 6, 43. https://doi.org/10.1186/1756-6606-6-43
  • Oswald, L. M., Wong, D. F., Zhou, Y., Kumar, A., Brasic, J., Alexander, M., Ye, W., Kuwabara, H., Hilton, J., & Wand, G. S. (2007). Impulsivity and chronic stress are associated with amphetamine-induced striatal dopamine release. NeuroImage, 36(1), 153–166. https://doi.org/10.1016/j.neuroimage.2007.01.055
  • Page, C. E., & Coutellier, L. (2019). Prefrontal excitatory/inhibitory balance in stress and emotional disorders: Evidence for over-inhibition. Neuroscience and Biobehavioral Reviews, 105, 39–51. https://doi.org/10.1016/j.neubiorev.2019.07.024
  • Page, C. E., Shepard, R., Heslin, K., & Coutellier, L. (2019). Prefrontal parvalbumin cells are sensitive to stress and mediate anxiety-related behaviors in female mice. Scientific Reports, 9(1), 19772. https://doi.org/10.1038/s41598-019-56424-9
  • Paxinos, G., & Franklin, K. B. J. (2008). Mouse brain in stereotaxic coordinates. Compact ( 3rd ed.). Academic.
  • Rogan, S. C., & Roth, B. L. (2011). Remote control of neuronal signaling. Pharmacological Reviews, 63(2), 291–315. https://doi.org/10.1124/pr.110.003020
  • Rymar, V. V., & Sadikot, A. F. (2007). Laminar fate of cortical GABAergic interneurons is dependent on both birthdate and phenotype. The Journal of Comparative Neurology, 501(3), 369–380. https://doi.org/10.1002/cne.21250
  • Samad, N., Saleem, A., Yasmin, F., & Shehzad, M. A. (2018). Quercetin protects against stress-induced anxiety- and depression-like behavior and improves memory in male mice. Physiological Research, 67(5), 795–808. https://doi.org/10.33549/physiolres.933776
  • Sarihi, A., Mirnajafi-Zadeh, J., Jiang, B., Sohya, K., Safari, M. S., Arami, M. K., Yanagawa, Y., & Tsumoto, T. (2012). Cell type-specific, presynaptic LTP of inhibitory synapses on fast-spiking GABAergic neurons in the mouse visual cortex. The Journal of Neuroscience, 32(38), 13189–13199. https://doi.org/10.1523/JNEUROSCI.1386-12.2012
  • Shepard, R., Page, C. E., & Coutellier, L. (2016). Sensitivity of the prefrontal GABAergic system to chronic stress in male and female mice: Relevance for sex differences in stress-related disorders. Neuroscience, 332, 1–12. https://doi.org/10.1016/j.neuroscience.2016.06.038
  • Sherwood, C. C., Raghanti, M. A., Stimpson, C. D., Bonar, C. J., de Sousa, A. A., Preuss, T. M., & Hof, P. R. (2007). Scaling of inhibitory interneurons in areas v1 and v2 of anthropoid primates as revealed by calcium-binding protein immunohistochemistry. Brain, Behavior and Evolution, 69(3), 176–195. https://doi.org/10.1159/000096986
  • Soumier, A., & Sibille, E. (2014). Opposing effects of acute versus chronic blockade of frontal cortex somatostatin-positive inhibitory neurons on behavioral emotionality in mice. Neuropsychopharmacology, 39(9), 2252–2262. https://doi.org/10.1038/npp.2014.76
  • Strekalova, T., Spanagel, R., Bartsch, D., Henn, F. A., & Gass, P. (2004). Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology, 29(11), 2007–2017. https://doi.org/10.1038/sj.npp.1300532
  • Taglialatela, G., Hogan, D., Zhang, W. R., & Dineley, K. T. (2009). Intermediate- and long-term recognition memory deficits in Tg2576 mice are reversed with acute calcineurin inhibition. Behavioural Brain Research, 200(1), 95–99. https://doi.org/10.1016/j.bbr.2008.12.034
  • Tremblay, R., Lee, S., & Rudy, B. (2016). GABAergic interneurons in the neocortex: From cellular properties to circuits. Neuron, 91(2), 260–292. https://doi.org/10.1016/j.neuron.2016.06.033
  • Winkelmann, A., Maggio, N., Eller, J., Caliskan, G., Semtner, M., Häussler, U., Jüttner, R., Dugladze, T., Smolinsky, B., Kowalczyk, S., Chronowska, E., Schwarz, G., Rathjen, F. G., Rechavi, G., Haas, C. A., Kulik, A., Gloveli, T., Heinemann, U., & Meier, J. C. (2014). Changes in neural network homeostasis trigger neuropsychiatric symptoms. The Journal of Clinical Investigation, 124(2), 696–711. https://doi.org/10.1172/JCI71472
  • Wohleb, E. S., Terwilliger, R., Duman, C. H., & Duman, R. S. (2018). Stress-induced neuronal colony stimulating factor 1 provokes microglia-mediated neuronal remodeling and depressive-like behavior. Biological Psychiatry, 83(1), 38–49. https://doi.org/10.1016/j.biopsych.2017.05.026
  • Zanos, P., Nelson, M. E., Highland, J. N., Krimmel, S. R., Georgiou, P., Gould, T. D., & Thompson, S. M. (2017). A negative allosteric modulator for alpha5 subunit-containing GABA receptors exerts a rapid and persistent antidepressant-like action without the side effects of the NMDA receptor antagonist ketamine in mice. eNeuro, 4(1), ENEURO.0285-16.2017. https://doi.org/10.1523/ENEURO.0285-16.2017
  • Zhou, Q. G., Zhu, L. J., Chen, C., Wu, H. Y., Luo, C. X., Chang, L., & Zhu, D. Y. (2011). Hippocampal neuronal nitric oxide synthase mediates the stress-related depressive behaviors of glucocorticoids by downregulating glucocorticoid receptor. Journal of Neuroscience, 31, 7579–7590. https://doi.org/10.1523/JNEUROSCI.0004-11.2011
  • Zhou, Z., Zhang, G., Li, X., Liu, X., Wang, N., Qiu, L., Liu, W., Zuo, Z., & Yang, J. (2015). Loss of phenotype of parvalbumin interneurons in rat prefrontal cortex is involved in antidepressant- and propsychotic-like behaviors following acute and repeated ketamine administration. Molecular Neurobiology, 51(2), 808–819. https://doi.org/10.1007/s12035-014-8798-2