Anti-manic effect of deep brain stimulation of the ventral tegmental area in an animal model of mania induced by methamphetamine.
bipolar disorder
deep brain stimulation
depression
dopamine
mania
methamphetamine
psychiatry
Journal
Bipolar disorders
ISSN: 1399-5618
Titre abrégé: Bipolar Disord
Pays: Denmark
ID NLM: 100883596
Informations de publication
Date de publication:
01 Apr 2024
01 Apr 2024
Historique:
medline:
1
4
2024
pubmed:
1
4
2024
entrez:
1
4
2024
Statut:
aheadofprint
Résumé
Treatment of refractory bipolar disorder (BD) is extremely challenging. Deep brain stimulation (DBS) holds promise as an effective treatment intervention. However, we still understand very little about the mechanisms of DBS and its application on BD. The present study aimed to investigate the behavioural and neurochemical effects of ventral tegmental area (VTA) DBS in an animal model of mania induced by methamphetamine (m-amph). Wistar rats were given 14 days of m-amph injections, and on the last day, animals were submitted to 20 min of VTA DBS in two different patterns: intermittent low-frequency stimulation (LFS) or continuous high-frequency stimulation (HFS). Immediately after DBS, manic-like behaviour and nucleus accumbens (NAc) phasic dopamine (DA) release were evaluated in different groups of animals through open-field tests and fast-scan cyclic voltammetry. Levels of NAc dopaminergic markers were evaluated by immunohistochemistry. M-amph induced hyperlocomotion in the animals and both DBS parameters reversed this alteration. M-amph increased DA reuptake time post-sham compared to baseline levels, and both LFS and HFS were able to block this alteration. LFS was also able to reduce phasic DA release when compared to baseline. LFS was able to increase dopamine transporter (DAT) expression in the NAc. These results demonstrate that both VTA LFS and HFS DBS exert anti-manic effects and modulation of DA dynamics in the NAc. More specifically the increase in DA reuptake driven by increased DAT expression may serve as a potential mechanism by which VTA DBS exerts its anti-manic effects.
Sections du résumé
BACKGROUND
BACKGROUND
Treatment of refractory bipolar disorder (BD) is extremely challenging. Deep brain stimulation (DBS) holds promise as an effective treatment intervention. However, we still understand very little about the mechanisms of DBS and its application on BD.
AIM
OBJECTIVE
The present study aimed to investigate the behavioural and neurochemical effects of ventral tegmental area (VTA) DBS in an animal model of mania induced by methamphetamine (m-amph).
METHODS
METHODS
Wistar rats were given 14 days of m-amph injections, and on the last day, animals were submitted to 20 min of VTA DBS in two different patterns: intermittent low-frequency stimulation (LFS) or continuous high-frequency stimulation (HFS). Immediately after DBS, manic-like behaviour and nucleus accumbens (NAc) phasic dopamine (DA) release were evaluated in different groups of animals through open-field tests and fast-scan cyclic voltammetry. Levels of NAc dopaminergic markers were evaluated by immunohistochemistry.
RESULTS
RESULTS
M-amph induced hyperlocomotion in the animals and both DBS parameters reversed this alteration. M-amph increased DA reuptake time post-sham compared to baseline levels, and both LFS and HFS were able to block this alteration. LFS was also able to reduce phasic DA release when compared to baseline. LFS was able to increase dopamine transporter (DAT) expression in the NAc.
CONCLUSION
CONCLUSIONS
These results demonstrate that both VTA LFS and HFS DBS exert anti-manic effects and modulation of DA dynamics in the NAc. More specifically the increase in DA reuptake driven by increased DAT expression may serve as a potential mechanism by which VTA DBS exerts its anti-manic effects.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Organisme : National Health and Medical Research Council
ID : APP1160472
Organisme : National Health and Medical Research Council
ID : GNT1156072
Organisme : National Health and Medical Research Council
ID : 2017131
Organisme : The Centre of Research Excellence for the Development of Innovative Therapies for Psychiatric Disorders
ID : GNT1153607
Informations de copyright
© 2024 The Authors. Bipolar Disorders published by John Wiley & Sons Ltd.
Références
Baldessarini RJ, Salvatore P, Khalsa HM, et al. Morbidity in 303 first‐episode bipolar I disorder patients. Bipolar Disord. 2010;12(3):264‐270.
Merikangas KR, Jin R, He JP, et al. Prevalence and correlates of bipolar spectrum disorder in the world mental health survey initiative. Arch Gen Psychiatry. 2011;68(3):241‐251.
Gitlin MJ. Antidepressants in bipolar depression: an enduring controversy. Int J Bipolar Disord. 2018;6(1):25.
Fountoulakis KN. Refractoriness in bipolar disorder: definitions and evidence‐based treatment. CNS Neurosci Ther. 2012;18(3):227‐237.
Schoeyen HK, Kessler U, Andreassen OA, et al. Treatment‐resistant bipolar depression: a randomized controlled trial of electroconvulsive therapy versus algorithm‐based pharmacological treatment. Am J Psychiatry. 2015;172(1):41‐51.
Ressler KJ, Mayberg HS. Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nat Neurosci. 2007;10(9):1116‐1124.
Fulton S, Pissios P, Manchon RP, et al. Leptin regulation of the mesoaccumbens dopamine pathway. Neuron. 2006;51(6):811‐822.
Rodríguez‐López C, Clascá F, Prensa L. The mesoaccumbens pathway: a retrograde labeling and single‐cell axon tracing analysis in the mouse. Front Neuroanat. 2017;11:25.
Coenen VA, Panksepp J, Hurwitz TA, Urbach H, Mädler B. Human medial forebrain bundle (MFB) and anterior thalamic radiation (ATR): imaging of two major subcortical pathways and the dynamic balance of opposite affects in understanding depression. J Neuropsychiatry Clin Neurosci. 2012;24(2):223‐236.
Holtzheimer PE 3rd, Mayberg HS. Deep brain stimulation for treatment‐resistant depression. Am J Psychiatry. 2010;167(12):1437‐1444.
Drobisz D, Damborská A. Deep brain stimulation targets for treating depression. Behav Brain Res. 2019;359:266‐273.
Gippert SM, Switala C, Bewernick BH, et al. Deep brain stimulation for bipolar disorder‐review and outlook. CNS Spectr. 2017;22(3):254‐257.
Mallet L, Mesnage V, Houeto JL, et al. Compulsions, Parkinson's disease, and stimulation. Lancet. 2002;360(9342):1302‐1304.
Breit S, Schulz JB, Benabid AL. Deep brain stimulation. Cell Tissue Res. 2004;318(1):275‐288.
Galati S, Mazzone P, Fedele E, et al. Biochemical and electrophysiological changes of substantia nigra pars reticulata driven by subthalamic stimulation in patients with Parkinson's disease. Eur J Neurosci. 2006;23(11):2923‐2928.
Gazit T, Friedman A, Lax E, et al. Programmed deep brain stimulation synchronizes VTA gamma band field potential and alleviates depressive‐like behavior in rats. Neuropharmacology. 2015;91:135‐141.
Grace AA, Bunney BS, Moore H, Todd CL. Dopamine‐cell depolarization block as a model for the therapeutic actions of antipsychotic drugs. Trends Neurosci. 1997;20(1):31‐37.
Aum DJ, Tierney TS. Deep brain stimulation: foundations and future trends. Front Biosci (Landmark ed). 2018;23:162‐182.
Friedman A, Deri I, Friedman Y, et al. Decoding of dopaminergic mesolimbic activity and depressive behavior. J Mol Neurosci. 2007;32(1):72‐79.
Friedman A, Frankel M, Flaumenhaft Y, et al. Programmed acute electrical stimulation of ventral tegmental area alleviates depressive‐like behavior. Neuropsychopharmacology. 2009;34(4):1057‐1066.
Hamani C, Nóbrega JN. Deep brain stimulation in clinical trials and animal models of depression. Eur J Neurosci. 2010;32(7):1109‐1117.
McClung CA, Sidiropoulou K, Vitaterna M, et al. Regulation of dopaminergic transmission and cocaine reward by the clock gene. Proc Natl Acad Sci USA. 2005;102(26):9377‐9381.
Feier G, Valvassori SS, Varela RB, et al. Lithium and valproate modulate energy metabolism in an animal model of mania induced by methamphetamine. Pharmacol Biochem Behav. 2013;103(3):589‐596.
Berk M, Dodd S, Kauer‐Sant'anna M, et al. Dopamine dysregulation syndrome: implications for a dopamine hypothesis of bipolar disorder. Acta Psychiatr Scand Suppl. 2007;434:41‐49.
Gerasimov MR, Ashby CR Jr, Gardner EL, Mills MJ, Brodie JD, Dewey SL. Gamma‐vinyl GABA inhibits methamphetamine, heroin, or ethanol‐induced increases in nucleus accumbens dopamine. Synapse. 1999;34(1):11‐19.
Kuhn DM, Angoa‐Pérez M, Thomas DM. Nucleus accumbens invulnerability to methamphetamine neurotoxicity. ILAR J. 2011;52(3):352‐365.
Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 7th ed. Elsevier; 2006.
Germano IM, Gracies JM, Weisz DJ, Tse W, Koller WC, Olanow CW. Unilateral stimulation of the subthalamic nucleus in Parkinson disease: a double‐blind 12‐month evaluation study. J Neurosurg. 2004;101(1):36‐42.
Kouzani AZ, Kale RP, Zarate‐Garza PP, Berk M, Walder K, Tye SJ. Validation of a portable low‐power deep brain stimulation device through anxiolytic effects in a laboratory rat model. IEEE Trans Neural Syst Rehabil Eng. 2017;25(9):1365‐1374.
Schindelin J, Arganda‐Carreras I, Frise E, et al. Fiji: an open‐source platform for biological‐image analysis. Nat Methods. 2012;9(7):676‐682.
Sharma AN, Fries GR, Galvez JF, et al. Modeling mania in preclinical settings: a comprehensive review. Prog Neuro‐Psychopharmacol Biol Psychiatry. 2016;66:22‐34.
Einat H. Different behaviors and different strains: potential new ways to model bipolar disorder. Neurosci Biobehav Rev. 2007;31(6):850‐857.
Menegas S, Dal‐Pont GC, Cararo JH, et al. Efficacy of folic acid as an adjunct to lithium therapy on manic‐like behaviors, oxidative stress and inflammatory parameters in an animal model of mania. Metab Brain Dis. 2020;35(2):413‐425.
Holtzheimer PE, Husain MM, Lisanby SH, et al. Subcallosal cingulate deep brain stimulation for treatment‐resistant depression: a multisite, randomised, sham‐controlled trial. Lancet Psychiatry. 2017;4(11):839‐849.
Coenen VA, Bewernick BH, Kayser S, et al. Superolateral medial forebrain bundle deep brain stimulation in major depression: a gateway trial. Neuropsychopharmacology. 2019;44(7):1224‐1232.
Perez‐Caballero L, Pérez‐Egea R, Romero‐Grimaldi C, et al. Early responses to deep brain stimulation in depression are modulated by anti‐inflammatory drugs. Mol Psychiatry. 2014;19(5):607‐614.
Perez SM, Shah A, Asher A, Lodge DJ. Hippocampal deep brain stimulation reverses physiological and behavioural deficits in a rodent model of schizophrenia. Int J Neuropsychopharmacol. 2013;16(6):1331‐1339.
Jang EY, Yang CH, Hedges DM, et al. The role of reactive oxygen species in methamphetamine self‐administration and dopamine release in the nucleus accumbens. Addict Biol. 2017;22(5):1304‐1315.
Xie Z, Miller GM. A receptor mechanism for methamphetamine action in dopamine transporter regulation in brain. J Pharmacol Exp Ther. 2009;330(1):316‐325.
Takeichi T, Hori O, Hattori T, Kiryu K, Zuka M, Kitamura O. Pre‐administration of low‐dose methamphetamine enhances movement and neural activity after high‐dose methamphetamine administration in the striatum. Neurosci Lett. 2019;703:119‐124.
Shepard JD, Chuang DT, Shaham Y, Morales M. Effect of methamphetamine self‐administration on tyrosine hydroxylase and dopamine transporter levels in mesolimbic and nigrostriatal dopamine pathways of the rat. Psychopharmacology. 2006;185(4):505‐513.
Lohani S, Martig AK, Underhill SM, et al. Burst activation of dopamine neurons produces prolonged post‐burst availability of actively released dopamine. Neuropsychopharmacology. 2018;43(10):2083‐2092.
Friedman A, Lax E, Abraham L, Tischler H, Yadid G. Abnormality of VTA local field potential in an animal model of depression was restored by patterned DBS treatment. Eur Neuropsychopharmacol. 2012;22(1):64‐71.
Branch SY, Beckstead MJ. Methamphetamine produces bidirectional, concentration‐dependent effects on dopamine neuron excitability and dopamine‐mediated synaptic currents. J Neurophysiol. 2012;108(3):802‐809.
Miller DR, Guenther DT, Maurer AP, Hansen CA, Zalesky A, Khoshbouei H. Dopamine transporter is a master regulator of dopaminergic neural network connectivity. J Neurosci. 2021;41(25):5453‐5470.
Greenwood TA, Alexander M, Keck PE, et al. Evidence for linkage disequilibrium between the dopamine transporter and bipolar disorder. Am J Med Genet. 2001;105(2):145‐151.
Anand A, Barkay G, Dzemidzic M, et al. Striatal dopamine transporter availability in unmedicated bipolar disorder. Bipolar Disord. 2011;13(4):406‐413.
Zhao M, Wang X, Deng J, et al. Globus pallidus internus electric high‐frequency stimulation modulates dopaminergic activity in the striatum of a rat model of Tourette syndrome. World Neurosurg. 2019;127:e881‐e887.
Zhang C, Wei H, Zhang Y, et al. Increased dopamine transporter levels following nucleus accumbens deep brain stimulation in methamphetamine use disorder: a case report. Brain Stimul. 2019;12(4):1055‐1057.
Nguyen MD, Venton BJ. Fast‐scan cyclic voltammetry for the characterization of rapid adenosine release. Comput Struct Biotechnol J. 2015;13:47‐54.
Oh Y, Heien ML, Park C, et al. Tracking tonic dopamine levels in vivo using multiple cyclic square wave voltammetry. Biosens Bioelectron. 2018;121:174‐182.