Antidepressant actions of lateral habenula deep brain stimulation differentially correlate with CaMKII/GSK3/AMPK signaling locally and in the infralimbic cortex

Behavioural Brain Research

Volumn 306, Issue , 2016, Pages 170-177

  Kim, Yesul ^a,b   Morath, Brooke ^a   Hu, Chunling ^a   Byrne, Linda K ^b   Sutor, Shari L ^a   Frye, Mark A ^a   Tye, Susannah J ^a,b,c  

^a MAYO CLINIC   (United States)

^b DEAKIN UNIVERSITY   (Australia)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

AMPK; CaMKII; Deep brain stimulation; GSK3; Lateral habenula; Treatment resistant depression

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II ALPHA; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II BETA; CORTICOTROPIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; DOWN REGULATION; FORCED SWIM TEST; HABENULA; INFRALIMBIC CORTEX; LATERAL HABENULA; MALE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; WESTERN BLOTTING; ANIMAL; DISEASE MODEL; DRUG EFFECTS; EXPLORATORY BEHAVIOR; LIMBIC CORTEX; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY; SIGNAL TRANSDUCTION; SWIMMING; TONIC IMMOBILITY; TREATMENT RESISTANT DEPRESSION; WISTAR RAT;

ADRENOCORTICOTROPIC HORMONE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; DEEP BRAIN STIMULATION; DEPRESSIVE DISORDER, TREATMENT-RESISTANT; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; GLYCOGEN SYNTHASE KINASE 3; HABENULA; IMMOBILITY RESPONSE, TONIC; LIMBIC LOBE; MALE; PHOSPHORYLATION; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SWIMMING;

EID: 84962262579     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2016.02.039     Document Type: Article

References (61)

1. Lecourtier L., Kelly P.H. A conductor hidden in the orchestra? Role of the habenular complex in monoamine transmission and cognition. Neurosci. Biobehav. Rev. 2007, 31:658-672.
2. Hikosaka O., Sesack S.R., Lecourtier L., Shepard P.D. Habenula crossroad between the basal ganglia and the limbic system. J. Neurosci. 2008, 28:11825-11829.
3. Pierucci M., Pitruzzella A., Valentino M., Zammit C., Muscat R., Benigno A., et al. Lateral habenula contribution in nicotine addiction: focus on dopamine, GABA and serotonin interactions. Malta Med. J. 2011, 23.
4. Belzung C., Willner P., Philippot P. Depression: from psychopathology to pathophysiology. Curr. Opin. Neurobiol. 2015, 30:24-30.
5. Gass N., Cleppien D., Zheng L., Schwarz A.J., Meyer-Lindenberg A., Vollmayr B., et al. Functionally altered neurocircuits in a rat model of treatment-resistant depression show prominent role of the habenula. Eur. Neuropsychopharmacol. 2014, 24:381-390.
6. Morris J., Smith K., Cowen P., Friston K., Dolan R. Covariation of activity in habenula and dorsal raphe nuclei following tryptophan depletion. Neuroimage 1999, 10:163-172.
7. Caldecott-Hazard S., Mazziotta J., Phelps M. Cerebral correlates of depressed behavior in rats, visualized using 14C-2-deoxyglucose autoradiography. J. Neurosci. 1988, 8:1951-1961.
8. Mirrione M.M., Schulz D., Lapidus K.A., Zhang S., Goodman W., Henn F.A. Increased metabolic activity in the septum and habenula during stress is linked to subsequent expression of learned helplessness behavior. Front. Hum. Neurosci. 2014, 8.
9. Li B., Piriz J., Mirrione M., Chung C., Proulx C.D., Schulz D., et al. Synaptic potentiation onto habenula neurons in the learned helplessness model of depression. Nature 2011, 470:535-539.
10. Shumake J., Edwards E., Gonzalez-Lima F. Opposite metabolic changes in the habenula and ventral tegmental area of a genetic model of helpless behavior. Brain Res. 2003, 963:274-281.
11. Yang L.-M., Hu B., Xia Y.-H., Zhang B.-L., Zhao H. Lateral habenula lesions improve the behavioral response in depressed rats via increasing the serotonin level in dorsal raphe nucleus. Behav. Brain Res. 2008, 188:84-90.
12. Amat J., Sparks P., Matus-Amat P., Griggs J., Watkins L., Maier S. The role of the habenular complex in the elevation of dorsal raphe nucleus serotonin and the changes in the behavioral responses produced by uncontrollable stress. Brain Res. 2001, 917:118-126.
13. Sourani D., Eitan R., Gordon N., Goelman G. The habenula couples the dopaminergic and the serotonergic systems: application to depression in Parkinson's disease. Eur. J. Neurosci. 2012, 36:2822-2829.
14. Omelchenko N., Bell R., Sesack S.R. Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area. Eur. J. Neurosci. 2009, 30:1239-1250.
15. Sartorius A., Kiening K.L., Kirsch P., von Gall C.C., Haberkorn U., Unterberg A.W., 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.
16. Li N., Liu R.-J., Dwyer J.M., Banasr M., Lee B., Son H., et al. Glutamate N-methyl-D-aspartate receptor antagonists rapidly reverse behavioral and synaptic deficits caused by chronic stress exposure. Biol. Psychiatry 2011, 69:754-761.
17. Li K., Zhou T., Liao L., Yang Z., Wong C., Henn F., et al. βCaMKII in lateral habenula mediates core symptoms of depression. Science 2013, 341:1016-1020.
18. Aizawa H., Kobayashi M., Tanaka S., Fukai T., Okamoto H. Molecular characterization of the subnuclei in rat habenula. J. Comp. Neurol. 2012, 520:4051-4066.
19. Christensen T., Jensen L., Bouzinova E.V., Wiborg O. Molecular profiling of the lateral habenula in a rat model of depression. PLoS One 2013, 8:e80666.
20. Wagner F., French L., Veh R.W. Transcriptomic-anatomic analysis of the mouse habenula uncovers a high molecular heterogeneity among neurons in the lateral complex, while gene expression in the medial complex largely obeys subnuclear boundaries. Brain Struct. Funct. 2014, 1-20.
21. Smillie K.J., Cousin M.A. The role of GSK3 in presynaptic function. Int. J. Alzheimers Dis. 2011, 2011.
22. Song B., Lai B., Zheng Z., Zhang Y., Luo J., Wang C., et al. Inhibitory phosphorylation of GSK-3 by CaMKII couples depolarization to neuronal survival. J. Biol. Chem. 2010, 285:41122-41134.
23. Zhu S., Wang J., Zhang Y., Li V., Kong J., He J., et al. Unpredictable chronic mild stress induces anxiety and depression-like behaviors and inactivates AMP-activated protein kinase in mice. Brain Res. 2014, 1576:81-90.
24. Maes M., Fišar Z., Medina M., Scapagnini G., Nowak G., Berk M. New drug targets in depression: inflammatory, cell-mediated immune, oxidative and nitrosative stress, mitochondrial, antioxidant, and neuroprogressive pathways And new drug candidates-Nrf2 activators and GSK-3 inhibitors. Inflammopharmacology 2012, 20:127-150.
25. Zhao Y., Shen J., Su H., Li B., Xing D., Du L. Chronic corticosterone injections induce a decrease of ATP levels and sustained activation of AMP-activated protein kinase in hippocampal tissues of male mice. Brain Res. 2008, 1191:148-156.
26. Drevets W.C., Savitz J., Trimble M. The subgenual anterior cingulate cortex in mood disorders. CNS Spectr. 2008, 13:663.
27. Mayberg H.S., Liotti M., Brannan S.K., McGinnis S., Mahurin R.K., Jerabek P.A., et al. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am. J. Psychiatry 1999, 156:675-682.
28. Lozano A.M., Mayberg H.S., Giacobbe P., Hamani C., Craddock R.C., Kennedy S.H. Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biol. Psychiatry 2008, 64:461-467.
29. Mayberg H.S., Lozano A.M., Voon V., McNeely H.E., Seminowicz D., Hamani C., et al. Deep brain stimulation for treatment-resistant depression. Neuron 2005, 45:651-660.
30. Puigdemont D., Portella M.J., Pérez-Egea R., Molet J., Gironell A., de Diego-Adeliño J., et al. A randomized double-blind crossover trial of deep brain stimulation of the subcallosal cingulate gyrus in patients with treatment-resistant depression: a pilot study of relapse prevention. J. Psychiatry Neurosci. 2015, 1:8872147.
31. Lammel S., Tye K., Warden M. Progress in understanding mood disorders: optogenetic dissection of neural circuits Genes. Brain Behav. 2014, 13:38-51.
32. Lammel S., Lim B.K., Ran C., Huang K.W., Betley M.J., Tye K.M., et al. Input-specific control of reward and aversion in the ventral tegmental area. Nature 2012, 491:212-217.
33. Vadovičová K., Gasparotti R. Reward and Adversity Processing Circuits, Their Competition and Interactions with Dopamine and Serotonin Signaling 2013, ScienceOpen Research, arXiv:1304.4201. https://www.scienceopen.com/document/vid?id=b08282eb-bb9a-40ef-9c13-cc15cc77349e, 10.14293/S2199-1006.1.SOR-LIFE.AEKZPZ.v1.
34. Veerakumar A., Challis C., Gupta P., Da J., Upadhyay A., Beck S.G., et al. Antidepressant-like effects of cortical deep brain stimulation coincide with pro-neuroplastic adaptations of serotonin systems. Biol. Psychiatry 2014, 76:203-212.
35. Ullsperger M., Von Cramon D.Y. Error monitoring using external feedback: specific roles of the habenular complex, the reward system, and the cingulate motor area revealed by functional magnetic resonance imaging. J. Neurosci. 2003, 23:4308-4314.
36. Shumake J., Gonzalez-Lima F. Brain systems underlying susceptibility to helplessness and depression. Behav. Cogn. Neurosci. Rev. 2003, 2:198-221.
37. Ago Y., Yano K., Araki R., Hiramatsu N., Kita Y., Kawasaki T., et al. Metabotropic glutamate 2/3 receptor antagonists improve behavioral and prefrontal dopaminergic alterations in the chronic corticosterone-induced depression model in mice. Neuropharmacology 2013, 65:29-38.
38. Iijima M., Ito A., Kurosu S., Chaki S. Pharmacological characterization of repeated corticosterone injection-induced depression model in rats. Brain Res. 2010, 1359:75-80.
39. Iwai T., Ohnuki T., Sasaki-Hamada S., Saitoh A., Sugiyama A., Oka J.-I. Glucagon-like peptide-2 but not imipramine exhibits antidepressant-like effects in ACTH-treated mice. Behav. Brain Res. 2013, 243:153-157.
40. Kitamura Y., Araki H., Gomita Y. Influence of ACTH on the effects of imipramine, desipramine and lithium on duration of immobility of rats in the forced swim test. Pharmacol. Biochem. Behav. 2002, 71:63-69.
41. Kitamura Y., Fujitani Y., Kitagawa K., Miyazaki T., Sagara H., Kawasaki H., et al. Effects of imipramine and bupropion on the duration of immobility of ACTH-treated rats in the forced swim test: involvement of the expression of 5-HT2A receptor mRNA. Biol. Pharm. Bull. 2008, 31:246-249.
42. Tokita K., Fujita Y., Yamaji T., Hashimoto K. Depressive-like behavior in adrenocorticotropic hormone-treated rats blocked by memantine. Pharmacol. Biochem. Behav. 2012, 102:329-334.
43. Walker A.J., Burnett S.A., Hasebe K., McGillivray J.A., Gray L.J., McGee S.L., et al. Chronic adrenocorticotrophic hormone treatment alters tricyclic antidepressant efficacy and prefrontal monoamine tissue levels. Behav. Brain Res. 2013, 242:76-83.
44. Meng H., Wang Y., Huang M., Lin W., Wang S., Zhang B. Chronic deep brain stimulation of the lateral habenula nucleus in a rat model of depression. Brain Res. 2011, 1422:32-38.
45. Martín-Blanco A., Serra-Blasco M., Pérez-Egea R., de Diego-Adeliño J., Carceller-Sindreu M., Puigdemont D., et al. Immediate cerebral metabolic changes induced by discontinuation of deep brain stimulation of subcallosal cingulate gyrus in treatment-resistant depression. J. Affect. Disord. 2015, 173:159-162.
46. Shumake J., Ilango A., Scheich H., Wetzel W., Ohl F.W. Differential neuromodulation of acquisition and retrieval of avoidance learning by the lateral habenula and ventral tegmental area. J. Neurosci. 2010, 30:5876-5883.
47. Warden M.R., Selimbeyoglu A., Mirzabekov J.J., Lo M., Thompson K.R., Kim S.-Y., et al. A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge. Nature 2012, 492:428-432.
48. Tao K., Matsuki N., Koyama R. AMP-activated protein kinase mediates activity-dependent axon branching by recruiting mitochondria to axon. Dev. Neurobiol. 2014, 74:557-573.
49. Vyazovskiy V.V., Cirelli C., Pfister-Genskow M., Faraguna U., Tononi G. Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat. Neurosci. 2008, 11:200-208.
50. Manji H.K., Duman R.S. Impairments of neuroplasticity and cellular resilience in severe mood disorders: implications for the development of novel therapeutics. Psychopharmacol. Bull. 2000, 35:5-49.
51. Manji H.K., Moore G.J., Rajkowska G., Chen G. Neuroplasticity and cellular resilience in mood disorders. Mol. Psychiatry 2000, 5:578-593.
52. Moylan S., Maes M., Wray N., Berk M. The neuroprogressive nature of major depressive disorder: pathways to disease evolution and resistance, and therapeutic implications. Mol. Psychiatry 2013, 18:595-606.
53. Potter W.B., O'riordan K.J., Barnett D., Osting S., Wagoner M., Burger C., et al. Metabolic regulation of neuronal plasticity by the energy sensor AMPK. PLoS One 2010, 5:e8996.
54. Soeiro-de-Souza M., Dias V., Figueira M., Forlenza O., Gattaz W., Zarate C., et al. Translating neurotrophic and cellular plasticity: from pathophysiology to improved therapeutics for bipolar disorder. Acta Psychiatr. Scand. 2012, 126:332-341.
55. Beurel E., Song L., Jope R. Inhibition of glycogen synthase kinase-3 is necessary for the rapid antidepressant effect of ketamine in mice. Mol. Psychiatry 2011, 16:1068-1070.
56. Veerakumar A., Berton O. Cellular mechanisms of deep brain stimulation: activity-dependent focal circuit reprogramming. Curr. Opin. Behav. Sci. 2015, 4:48-55.
57. Shabel S.J., Proulx C.D., Piriz J., Malinow R. GABA/glutamate co-release controls habenula output and is modified by antidepressant treatment. Science 2014, 345:1494-1498.
58. Vialou V., Feng J., Robison A.J., Nestler E.J. Epigenetic mechanisms of depression and antidepressants action. Annu. Rev. Pharmacool. Toxicol. 2013, 53:59.
59. Matsumoto M., Hikosaka O. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 2009, 459:837-841.
60. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Academic Press/Elsevier, Amsterdam;Boston. 6th edn.
61. Kim Y., McGee S., Czeczor J.K., Walker A.J., Kale R., Kouzani A., Walder K., Berk M., Tye S.J. Nucleus accumbens deep brain stimulation efficacy in ACTH pretreated rats: alterations in mitochondrial function relate to antidepressant-like effects. Transl. Psychiatry 2016, (in press).