The Antidepressant Effect of Nucleus Accumbens Deep Brain Stimulation is Mediated by Parvalbumin-positive Interneurons in the Dorsal Dentate Gyrus

Overview

Journal Neurobiol Stress

Date 2022 Dec 19

PMID 36532368

Authors

Hong Zhou

Jiayu Zhu

Jie Jia

Wei Xiang

Hualing Peng

Yuejin Zhang

Bo Liu

Yangling Mu

Yisheng Lu

Affiliations

Soon will be listed here.

Abstract

The nucleus accumbens (NAc) is a crucial region in the reward circuit and is related to anhedonia, the pivotal symptom of major depression disorder (MDD). Deep brain stimulation (DBS) of NAc has been identified as an effective treatment for severe refractory major depression; however, the underlying mechanism of NAc-DBS in MDD treatment remains elusive. Using the chronic unpredictable mild stress (CUMS) mouse model, we found NAc-DBS rescued depression-like behaviors, and reversed high gamma oscillation reduction and neurogenesis impairment in the dorsal dentate gyrus. Inactivation of parvalbumin (PV)-positive interneurons (PVI) in the dorsal DG led to depression-like behavior and decreased adult neurogenesis. Further investigation elucidated the VTA-DG GABAergic projection and CA1-NAc projection might jointly participate in NAc-DBS therapeutic mechanism. Disinhibition of the VTA-DG GABAergic projection had an antidepressant effect, and inhibition of the CA1-NAc projection reduced the antidepressant effect of DBS-NAc. Moreover, disinhibiting the VTA-DG GABAergic projection or activating the CA1-NAc projection could increase PVI activity in the dorsal DG. These results showed PVI in the dorsal DG as an essential target in depression and NAc-DBS antidepressant mechanisms.

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References

Lim L, Janssen M, Kocabicak E, Temel Y . The antidepressant effects of ventromedial prefrontal cortex stimulation is associated with neural activation in the medial part of the subthalamic nucleus. Behav Brain Res. 2014; 279:17-21. DOI: 10.1016/j.bbr.2014.11.008. View

Bewernick B, Hurlemann R, Matusch A, Kayser S, Grubert C, Hadrysiewicz B . Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression. Biol Psychiatry. 2009; 67(2):110-6. DOI: 10.1016/j.biopsych.2009.09.013. View

Minichino A, Bersani F, Capra E, Pannese R, Bonanno C, Salviati M . ECT, rTMS, and deepTMS in pharmacoresistant drug-free patients with unipolar depression: a comparative review. Neuropsychiatr Dis Treat. 2012; 8:55-64. PMC: 3280107. DOI: 10.2147/NDT.S27025. View

Jakobs M, Fomenko A, Lozano A, Kiening K . Cellular, molecular, and clinical mechanisms of action of deep brain stimulation-a systematic review on established indications and outlook on future developments. EMBO Mol Med. 2019; 11(4). PMC: 6460356. DOI: 10.15252/emmm.201809575. View

Wacker J, Dillon D, Pizzagalli D . The role of the nucleus accumbens and rostral anterior cingulate cortex in anhedonia: integration of resting EEG, fMRI, and volumetric techniques. Neuroimage. 2009; 46(1):327-37. PMC: 2686061. DOI: 10.1016/j.neuroimage.2009.01.058. View

Noda Y, Zomorrodi R, Saeki T, Rajji T, Blumberger D, Daskalakis Z . Resting-state EEG gamma power and theta-gamma coupling enhancement following high-frequency left dorsolateral prefrontal rTMS in patients with depression. Clin Neurophysiol. 2017; 128(3):424-432. DOI: 10.1016/j.clinph.2016.12.023. View

Yi Y, Song Y, Lu Y . Parvalbumin Interneuron Activation-Dependent Adult Hippocampal Neurogenesis Is Required for Treadmill Running to Reverse Schizophrenia-Like Phenotypes. Front Cell Dev Biol. 2020; 8:24. PMC: 7010605. DOI: 10.3389/fcell.2020.00024. View

Bremner J, Narayan M, Anderson E, Staib L, Miller H, Charney D . Hippocampal volume reduction in major depression. Am J Psychiatry. 2000; 157(1):115-8. DOI: 10.1176/ajp.157.1.115. View

Alvarez D, Giacomini D, Yang S, Trinchero M, Temprana S, Buttner K . A disynaptic feedback network activated by experience promotes the integration of new granule cells. Science. 2016; 354(6311):459-465. DOI: 10.1126/science.aaf2156. View

10.

Martisova E, Solas M, Horrillo I, Ortega J, Meana J, Tordera R . Long lasting effects of early-life stress on glutamatergic/GABAergic circuitry in the rat hippocampus. Neuropharmacology. 2012; 62(5-6):1944-53. DOI: 10.1016/j.neuropharm.2011.12.019. View

11.

Malberg J, Eisch A, Nestler E, Duman R . Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci. 2000; 20(24):9104-10. PMC: 6773038. View

12.

Filipovic D, Stanisavljevic A, Jasnic N, Bernardi R, Inta D, Peric I . Chronic Treatment with Fluoxetine or Clozapine of Socially Isolated Rats Prevents Subsector-Specific Reduction of Parvalbumin Immunoreactive Cells in the Hippocampus. Neuroscience. 2017; 371:384-394. DOI: 10.1016/j.neuroscience.2017.12.020. View

13.

Hill A, Sahay A, Hen R . Increasing Adult Hippocampal Neurogenesis is Sufficient to Reduce Anxiety and Depression-Like Behaviors. Neuropsychopharmacology. 2015; 40(10):2368-78. PMC: 4538351. DOI: 10.1038/npp.2015.85. View

14.

Amilhon B, Huh C, Manseau F, Ducharme G, Nichol H, Adamantidis A . Parvalbumin Interneurons of Hippocampus Tune Population Activity at Theta Frequency. Neuron. 2015; 86(5):1277-89. DOI: 10.1016/j.neuron.2015.05.027. View

15.

Zou D, Chen L, Deng D, Jiang D, Dong F, McSweeney C . DREADD in parvalbumin interneurons of the dentate gyrus modulates anxiety, social interaction and memory extinction. Curr Mol Med. 2016; 16(1):91-102. PMC: 4997952. DOI: 10.2174/1566524016666151222150024. View

16.

Schlaepfer T, Cohen M, Frick C, Kosel M, Brodesser D, Axmacher N . Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology. 2007; 33(2):368-77. DOI: 10.1038/sj.npp.1301408. View

17.

Vaden R, Gonzalez J, Tsai M, Niver A, Fusilier A, Griffith C . Parvalbumin interneurons provide spillover to newborn and mature dentate granule cells. Elife. 2020; 9. PMC: 7326496. DOI: 10.7554/eLife.54125. View

18.

Zhang H, He X, Mei Y, Ling Q . Ablation of ErbB4 in parvalbumin-positive interneurons inhibits adult hippocampal neurogenesis through down-regulating BDNF/TrkB expression. J Comp Neurol. 2018; 526(15):2482-2492. DOI: 10.1002/cne.24506. View

19.

Nestler E, Carlezon Jr W . The mesolimbic dopamine reward circuit in depression. Biol Psychiatry. 2006; 59(12):1151-9. DOI: 10.1016/j.biopsych.2005.09.018. View

20.

Peric I, Stanisavljevic A, Inta D, Gass P, Lang U, Borgwardt S . Tianeptine antagonizes the reduction of PV+ and GAD67 cells number in dorsal hippocampus of socially isolated rats. Prog Neuropsychopharmacol Biol Psychiatry. 2018; 89:386-399. DOI: 10.1016/j.pnpbp.2018.10.013. View