Electrical stimulation alleviates depressive-like behaviors of rats: Investigation of brain targets and potential mechanisms

Translational Psychiatry

Volumn 5, Issue 3, 2015, Pages

  Lim, L W ^a,b,c,d   Prickaerts, J ^b   Huguet, G ^e   Kadar, E ^e   Hartung, H ^c   Sharp, T ^c   Temel, Y ^b  

^a SUNWAY UNIVERSITY   (Malaysia)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e UNIVERSITY OF GIRONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN C FOS; SEROTONIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDEPRESSANT ACTIVITY; ANXIETY; ARTICLE; BRAIN DEPTH STIMULATION; CHRONIC UNPREDICTABLE STRESS; CINGULATE GYRUS; CONTROLLED STUDY; DEPRESSION; DORSAL RAPHE NUCLEUS; ELECTROPHYSIOLOGY; FORCED SWIM TEST; HABENULA; MALE; MOTIVATION; NONHUMAN; NUCLEUS ACCUMBENS; PROTEIN EXPRESSION; RAT; SEROTONINERGIC NERVE CELL; VENTRAL TEGMENTUM; VENTROMEDIAL PREFRONTAL CORTEX; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; BRAIN; DISEASE MODEL; METABOLISM; PATHOPHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DEEP BRAIN STIMULATION; DEPRESSION; DISEASE MODELS, ANIMAL; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN;

EID: 84989917980     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.24     Document Type: Article

References (94)

1. Kessler RC, Berglund P, Demler O, Jin R, Koretz D, Merikangas KR et al. The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). JAMA 2003; 289: 3095-3105.
2. Alonso J, Angermeyer MC, Bernert S, Bruffaerts R, Brugha TS, Bryson H et al. Prevalence of mental disorders in Europe: results from the European Study of the Epidemiology of Mental Disorders (ESEMeD) project. Acta Psychiatr Scand Suppl 2004; 420: 21-27.
3. American Psychiatric Association. Practice guideline for the treatment of patients with major depressive disorder (revision). Am J Psychiatry 2002; 157: 1-45.
4. Temel Y, Hescham SA, Jahanshahi A, Janssen ML, Tan SK, van Overbeeke JJ et al. Neuromodulation in psychiatric disorders. Int Rev Neurobiol 2012; 107: 283-314.
5. Temel Y, Lim LW. Neurosurgical treatments of depression. Curr Top Behav Neurosci 2013; 14: 327-339.
6. Kennedy SH, Giacobbe P, Rizvi SJ, Placenza FM, Nishikawa Y, Mayberg HS et al. Deep brain stimulation for treatment-resistant depression: follow-up after 3 to 6 years. Am J Psychiatry 2011; 168: 502-510.
7. Lozano AM, Mayberg HS, Giacobbe P, Hamani C, Craddock RC, Kennedy SH. Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biol Psychiatry 2008; 64: 461-467.
8. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C et al. Deep brain stimulation for treatment-resistant depression. Neuron 2005; 45: 651-660.
9. Schlaepfer TE, Cohen MX, Frick C, Kosel M, Brodesser D, Axmacher N et al. Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 2007; 33: 368-377.
10. Schlaepfer TE, Cohen MX, Frick C, Kosel M, Brodesser D, Axmacher N et al. Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 2008; 33: 368-377.
11. Covington HE 3rd, Lobo MK, Maze I, Vialou V, Hyman JM, Zaman S et al. Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. J Neurosci 2010; 30: 16082-16090.
12. Falowski SM, Sharan A, Reyes BA, Sikkema C, Szot P, Van Bockstaele EJ. An evaluation of neuroplasticity and behavior following deep brain stimulation of the nucleus accumbens in an animal model of depression. Neurosurgery 2011; 69: 1281-1290.
13. Hamani C, Diwan M, Macedo CE, Brandao ML, Shumake J, Gonzalez-Lima F et al. Antidepressant-like effects of medial prefrontal cortex deep brain stimulation in rats. Biol Psychiatry 2010; 67: 117-124.
14. Hamani C, Machado DC, Hipolide DC, Dubiela FP, Suchecki D, Macedo CE et al. Deep brain stimulation reverses anhedonic-like behavior in a chronic model of depression: role of serotonin and brain derived neurotrophic factor. Biol Psychiatry 2012; 71: 30-35.
15. Lim LW, Janssen ML, 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.
16. Malone DA Jr., Dougherty DD, Rezai AR, Carpenter LL, Friehs GM, Eskandar EN et al. Deep brain stimulation of the ventral capsule/ventral striatum for treatmentresistant depression. Biol Psychiatry 2009; 65: 267-275.
17. Sartorius A, Kiening KL, Kirsch P, von Gall CC, Haberkorn U, Unterberg AW et al. Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol Psychiatry 2010; 67: e9-e11.
18. Li B, Piriz J, Mirrione M, Chung C, Proulx CD, Schulz D et al. Synaptic potentiation onto habenula neurons in the learned helplessness model of depression. Nature 2011; 470: 535-539.
19. Friedman A, Frankel M, Flaumenhaft Y, Merenlender A, Pinhasov A, Feder Y et al. Programmed acute electrical stimulation of ventral tegmental area alleviates depressive-like behavior. Neuropsychopharmacology 2009; 34: 1057-1066.
20. Mayberg HS. Limbic-cortical dysregulation: a proposed model of depression. J Neuropsychiatry Clin Neurosci 1997; 9: 471-481.
21. Mayberg HS, Liotti M, Brannan SK, McGinnis S, Mahurin RK, Jerabek PA et al. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 1999; 156: 675-682.
22. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition 2013.
23. Barnes NM, Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 1999; 38: 1083-1152.
24. Hestermann D, Temel Y, Blokland A, Lim LW. Acute serotonergic treatment changes the relation between anxiety and HPA-Axis functioning and periaqueductal gray activation. Behav Brain Res 2014; 273: 155-165.
25. Lim LW, Blokland A, Tan S, Vlamings R, Sesia T, Aziz-Mohammadi M et al. Attenuation of fear-like response by escitalopram treatment after electrical stimulation of the midbrain dorsolateral periaqueductal gray. Exp Neurol 2010; 226: 293-300.
26. Tan S, Vlamings R, Lim L, Sesia T, Janssen ML, Steinbusch HW et al. Experimental deep brain stimulation in animal models. Neurosurgery 2010; 67: 1073-1079.
27. Paxinos G, Watson C. The rat brain in stereotaxic coordinates, 6th Edition. Academic Press of Elsevier; China, 2007.
28. Lim LW, Blokland A, Visser-Vandewalle V, Vlamings R, Sesia T, Steinbusch H et al. High-frequency stimulation of the dorsolateral periaqueductal gray and ventromedial hypothalamus fails to inhibit panic-like behaviour. Behav Brain Res 2008; 193: 197-203.
29. Temel Y, Boothman LJ, Blokland A, Magill PJ, Steinbusch HW, Visser-Vandewalle V et al. Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc Natl Acad Sci USA 2007; 104: 17087-17092.
30. Prickaerts J, Raaijmakers W, Blokland A. Effects of myocardial infarction and captopril therapy on anxiety-related behaviors in the rat. Physiol Behav 1996; 60: 43-50.
31. Lim LW, Temel Y, Visser-Vandewalle V, Steinbusch H, Schruers K, Hameleers R et al. Effect of buspirone on the behavioral regulation of rats in low versus high anxiety conditions. Arzneimittelforschung 2008; 58: 269-276.
32. van der Plasse G, Schrama R, van Seters SP, Vanderschuren LJ, Westenberg HG. Deep brain stimulation reveals a dissociation of consummatory and motivated behaviour in the medial and lateral nucleus accumbens shell of the rat. PLoS One 2012; 7: e33455.
33. Blokland A, Lieben C, Deutz NE. Anxiogenic and depressive-like effects, but no cognitive deficits, after repeated moderate tryptophan depletion in the rat. J Psychopharmacol 2002; 16: 39-49.
34. Cryan JF, Valentino RJ, Lucki I. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 2005; 29: 547-569.
35. Lucas G, Rymar VV, Du J, Mnie-Filali O, Bisgaard C, Manta S et al. Serotonin(4) (5-HT(4)) receptor agonists are putative antidepressants with a rapid onset of action. Neuron 2007; 55: 712-725.
36. Mateus-Pinheiro A, Pinto L, Bessa JM, Morais M, Alves ND, Monteiro S et al. Sustained remission from depressive-like behavior depends on hippocampal neurogenesis. Transl Psychiatry 2013; 3: e210.
37. Hartung H, Tan SK, Steinbusch HM, Temel Y, Sharp T. High-frequency stimulation of the subthalamic nucleus inhibits the firing of juxtacellular labelled 5-HTcontaining neurones. Neuroscience 2011; 186: 135-145.
38. Jahanshahi A, Lim LW, Steinbusch HW, Visser-Vandewalle V, Temel Y. Buspironeinduced changes in the serotonergic and non-serotonergic cells in the dorsal raphe nucleus of rats. Neurosci Lett 2010; 473: 136-140.
39. Lim LW, Temel Y, Sesia T, Vlamings R, Visser-Vandewalle V, Steinbusch HW et al. Buspirone induced acute and chronic changes of neural activation in the periaqueductal gray of rats. Neuroscience 2008; 155: 164-173.
40. Hamani C, Nobrega JN. Preclinical studies modeling deep brain stimulation for depression. Biol Psychiatry 2012; 72: 916-923.
41. Cryan JF, Markou A, Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 2002; 23: 238-245.
42. Forbes NF, Stewart CA, Matthews K, Reid IC. Chronic mild stress and sucrose consumption: validity as a model of depression. Physiol Behav 1996; 60: 1481-1484.
43. Fawcett J, Clark DC, Scheftner WA, Gibbons RD. Assessing anhedonia in psychiatric patients. Arch Gen Psychiatry 1983; 40: 79-84.
44. Hamani C, Diwan M, Isabella S, Lozano AM, Nobrega JN. Effects of different stimulation parameters on the antidepressant-like response of medial prefrontal cortex deep brain stimulation in rats. J Psychiatr Res 2010; 44: 683-687.
45. Kalen P, Strecker RE, Rosengren E, Bjorklund A. Regulation of striatal serotonin release by the lateral habenula-dorsal raphe pathway in the rat as demonstrated by in vivo microdialysis: role of excitatory amino acids and GABA. Brain Res 1989; 492: 187-202.
46. Do-Monte FH, Rodriguez-Romaguera J, Rosas-Vidal LE, Quirk GJ. Deep brain stimulation of the ventral striatum increases BDNF in the fear extinction circuit. Front Behav Neurosci 2013; 7: 102.
47. van Dijk A, Klompmakers AA, Feenstra MG, Denys D. Deep brain stimulation of the accumbens increases dopamine, serotonin, and noradrenaline in the prefrontal cortex. J Neurochem 2012; 123: 897-903.
48. Sesia T, Bulthuis V, Tan S, Lim LW, Vlamings R, Blokland A et al. Deep brain stimulation of the nucleus accumbens shell increases impulsive behavior and tissue levels of dopamine and serotonin. Exp Neurol 2010; 225: 302-309.
49. Quirk GJ, Beer JS. Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr Opin Neurobiol 2006; 16: 723-727.
50. Price JL, Drevets WC. Neurocircuitry of mood disorders. Neuropsychopharmacology 2010; 35: 192-216.
51. Radley JJ, Arias CM, Sawchenko PE. Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress. J Neurosci 2006; 26: 12967-12976.
52. Drevets WC, Price JL, Furey ML. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct 2008; 213: 93-118.
53. Drevets WC, Price JL, Simpson JR Jr., Todd RD, Reich T, Vannier M et al. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 1997; 386: 824-827.
54. Franklin TB, Saab BJ, Mansuy IM. Neural mechanisms of stress resilience and vulnerability. Neuron 2012; 75: 747-761.
55. Etkin A, Wager TD. Functional neuroimaging of anxiety: a meta-Analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 2007; 164: 1476-1488.
56. Hayes JP, Hayes SM, Mikedis AM. Quantitative meta-Analysis of neural activity in posttraumatic stress disorder. Biol Mood Anxiety Disord 2012; 2: 9.
57. Drevets WC, Ongur D, Price JL. Neuroimaging abnormalities in the subgenual prefrontal cortex: implications for the pathophysiology of familial mood disorders. Mol Psychiatry 1998; 3: 220-226, 190-221.
58. van Harmelen AL, van Tol MJ, Dalgleish T, van der Wee NJ, Veltman DJ, Aleman A et al. Hypoactive medial prefrontal cortex functioning in adults reporting childhood emotional maltreatment. Soc Cogn Affect Neurosci 2014; 9: 2026-2033.
59. Adamec R, Toth M, Haller J, Halasz J, Blundell J. A comparison of activation patterns of cells in selected prefrontal cortical and amygdala areas of rats which are more or less anxious in response to predator exposure or submersion stress. Physiol Behav 2012; 105: 628-638.
60. Chen BT, Yau HJ, Hatch C, Kusumoto-Yoshida I, Cho SL, Hopf FW et al. Rescuing cocaine-induced prefrontal cortex hypoactivity prevents compulsive cocaine seeking. Nature 2013; 496: 359-362.
61. Isserles M, Shalev AY, Roth Y, Peri T, Kutz I, Zlotnick E et al. Effectiveness of deep transcranial magnetic stimulation combined with a brief exposure procedure in post-traumatic stress disorder-A pilot study. Brain Stimul 2013; 6: 377-383.
62. Liu A, Jain N, Vyas A, Lim LW. Ventromedial prefrontal cortex stimulation enhances memory and hippocampal neurogenesis in the middle-Aged rats. Elife 2015; Mar 13;4. doi:10.7554/eLife.04803.
63. Euston DR, Gruber AJ, McNaughton BL. The role of medial prefrontal cortex in memory and decision making. Neuron 2012; 76: 1057-1070.
64. Heidbreder CA, Groenewegen HJ. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci Biobehav Rev 2003; 27: 555-579.
65. Hoover WB, Vertes RP. Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 2007; 212: 149-179.
66. Vertes RP, Hoover WB, Szigeti-Buck K, Leranth C. Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res Bull 2007; 71: 601-609.
67. Drevets WC. Functional anatomical abnormalities in limbic and prefrontal cortical structures in major depression. Prog Brain Res 2000; 126: 413-431.
68. Dolan RJ, Bench CJ, Brown RG, Scott LC, Friston KJ, Frackowiak RS. Regional cerebral blood flow abnormalities in depressed patients with cognitive impairment. J Neurol Neurosurg Psychiatry 1992; 55: 768-773.
69. Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-Analysis of neuroimaging studies. Neuroimage 2009; 44: 489-501.
70. Liotti M, Mayberg HS, Brannan SK, McGinnis S, Jerabek P, Fox PT. Differential limbic-cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders. Biol Psychiatry 2000; 48: 30-42.
71. Moers-Hornikx VM, Sesia T, Basar K, Lim LW, Hoogland G, Steinbusch HW et al. Cerebellar nuclei are involved in impulsive behaviour. Behav Brain Res 2009; 203: 256-263.
72. Moers-Hornikx VM, Vles JS, Lim LW, Ayyildiz M, Kaplan S, Gavilanes AW et al. Periaqueductal grey stimulation induced panic-like behaviour is accompanied by deactivation of the deep cerebellar nuclei. Cerebellum 2011; 10: 61-69.
73. Heath RG, Harper JW. Ascending projections of the cerebellar fastigial nucleus to the hippocampus, amygdala, and other temporal lobe sites: evoked potential and histological studies in monkeys and cats. Exp Neurol 1974; 45: 268-287.
74. Lu X, Miyachi S, Takada M. Anatomical evidence for the involvement of medial cerebellar output from the interpositus nuclei in cognitive functions. Proc Natl Acad Sci USA 2012; 109: 18980-18984.
75. Phelps EA. Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 2004; 14: 198-202.
76. Phelps EA, Delgado MR, Nearing KI, LeDoux JE. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 2004; 43: 897-905.
77. Hikosaka O. The habenula: from stress evasion to value-based decision-making. Nat Rev Neurosci 2010; 11: 503-513.
78. Reisine TD, Soubrie P, Artaud F, Glowinski J. Involvement of lateral habenuladorsal raphe neurons in the differential regulation of striatal and nigral serotonergic transmission cats. J Neurosci 1982; 2: 1062-1071.
79. Morris JS, Smith KA, Cowen PJ, Friston KJ, Dolan RJ. Covariation of activity in habenula and dorsal raphe nuclei following tryptophan depletion. Neuroimage 1999; 10: 163-172.
80. Hajos M, Gartside SE, Varga V, Sharp T. In vivo inhibition of neuronal activity in the rat ventromedial prefrontal cortex by midbrain-raphe nuclei: role of 5-HT1A receptors. Neuropharmacology 2003; 45: 72-81.
81. Varga V, Szekely AD, Csillag A, Sharp T, Hajos M. Evidence for a role of GABA interneurones in the cortical modulation of midbrain 5-hydroxytryptamine neurones. Neuroscience 2001; 106: 783-792.
82. Hamani C, Amorim BO, Wheeler AL, Diwan M, Driesslein K, Covolan L et al. Deep brain stimulation in rats: different targets induce similar antidepressant-like effects but influence different circuits. Neurobiol Dis 2014; 71: 205-214.
83. Hajos M, Richards CD, Szekely AD, Sharp T. An electrophysiological and neuroanatomical study of the medial prefrontal cortical projection to the midbrain raphe nuclei in the rat. Neuroscience 1998; 87: 95-108.
84. Liu R, Jolas T, Aghajanian G. Serotonin 5-HT(2) receptors activate local GABA inhibitory inputs to serotonergic neurons of the dorsal raphe nucleus. Brain Res 2000; 873: 34-45.
85. Allers KA, Sharp T. Neurochemical and anatomical identification of fast-And slow-firing neurones in the rat dorsal raphe nucleus using juxtacellular labelling methods in vivo. Neuroscience 2003; 122: 193-204.
86. Jacobs BL, Azmitia EC. Structure and function of the brain serotonin system. Physiol Rev 1992; 72: 165-229.
87. Navailles S, Benazzouz A, Bioulac B, Gross C, De Deurwaerdere P. High-frequency stimulation of the subthalamic nucleus and L-3,4-dihydroxyphenylalanine inhibit in vivo serotonin release in the prefrontal cortex and hippocampus in a rat model of Parkinson's disease. J Neurosci 2010; 30: 2356-2364.
88. Tan SK, Hartung H, Visser-Vandewalle V, Steinbusch HW, Temel Y, Sharp T. A combined in vivo neurochemical and electrophysiological analysis of the effect of high-frequency stimulation of the subthalamic nucleus on 5-HT transmission. Exp Neurol 2012; 233: 145-153.
89. Juckel G, Mendlin A, Jacobs BL. Electrical stimulation of rat medial prefrontal cortex enhances forebrain serotonin output: implications for electroconvulsive therapy and transcranial magnetic stimulation in depression. Neuropsychopharmacology 1999; 21: 391-398.
90. Liu RJ, Lambe EK, Aghajanian GK. Somatodendritic autoreceptor regulation of serotonergic neurons: dependence on L-tryptophan and tryptophan hydroxylaseactivating kinases. Eur J Neurosci 2005; 21: 945-958.
91. Heinrich R, Cromarty SI, Horner M, Edwards DH, Kravitz EA. Autoinhibition of serotonin cells: an intrinsic regulatory mechanism sensitive to the pattern of usage of the cells. Proc Natl Acad Sci USA 1999; 96: 2473-2478.
92. Araragi N, Mlinar B, Baccini G, Gutknecht L, Lesch KP, Corradetti R. Conservation of 5-HT1A receptor-mediated autoinhibition of serotonin (5-HT) neurons in mice with altered 5-HT homeostasis. Front Pharmacol 2013; 4: 97.
93. Levine ES, Jacobs BL. Neurochemical afferents controlling the activity of serotonergic neurons in the dorsal raphe nucleus: microiontophoretic studies in the awake cat. J Neurosci 1992; 12: 4037-4044.
94. Bagdy E, Kiraly I, Harsing LG Jr. Reciprocal innervation between serotonergic and GABAergic neurons in raphe nuclei of the rat. Neurochem Res 2000; 25: 1465-1473.