Antidepressant-like effects of cortical deep brain stimulation coincide with pro-neuroplastic adaptations of serotonin systems

Biological Psychiatry

Volumn 76, Issue 3, 2014, Pages 203-212

  Veerakumar, Avin ^a,c   Challis, Collin ^a   Gupta, Preetika ^a   Da, Jennifer ^a   Upadhyay, Aseem ^a   Beck, Sheryl G ^a,b   Berton, Olivier ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Deep brain stimulation; depression; dorsal raphe; neuroplasticity; prefrontal cortex; social defeat

Indexed keywords

POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN C FOS; SEROTONIN; STAINLESS STEEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY LABELING; ANTIDEPRESSANT ACTIVITY; ARTICLE; BRAIN DEPTH STIMULATION; CELL DENSITY; CELL FUNCTION; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; DEPRESSION; DORSAL RAPHE NUCLEUS; ELECTRODE; ELECTROPHYSIOLOGY; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MORPHOMETRICS; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; ONCOGENE C FOS; PATCH CLAMP TECHNIQUE; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRIFORM CORTEX; SEROTONINERGIC SYSTEM; SOCIAL AVOIDANCE BEHAVIOR; SOCIAL INTERACTION; SOCIAL INTERACTION TEST; SOCIAL STRESS; SYNAPTOSOME; THREE DIMENSIONAL IMAGING; VENTROMEDIAL PREFRONTAL CORTEX; WHOLE CELL PATCH CLAMP; ADAPTATION; ANIMAL; BRAIN; C57BL MOUSE; INHIBITORY POSTSYNAPTIC POTENTIAL; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; SEROTONINERGIC NERVE CELL; TRANSGENIC MOUSE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BRAIN; DEEP BRAIN STIMULATION; DEPRESSION; DORSAL RAPHE NUCLEUS; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PREFRONTAL CORTEX; SEROTONERGIC NEURONS;

EID: 84904063304     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.12.009     Document Type: Article

References (53)

1. H.S. Mayberg, A.M. Lozano, V. Voon, H.E. McNeely, D. Seminowicz, and C. Hamani et al. Deep brain stimulation for treatment-resistant depression Neuron 45 2005 651 660
2. A.M. Lozano, H.S. Mayberg, P. Giacobbe, C. Hamani, R.C. Craddock, and S.H. Kennedy Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression Biol Psychiatry 64 2008 461 467
3. P.E. Holtzheimer, M.E. Kelley, R.E. Gross, M.M. Filkowski, S.J. Garlow, and A. Barrocas et al. Subcallosal cingulate deep brain stimulation for treatment-resistant unipolar and bipolar depression Arch Gen Psychiatry 69 2012 150 158
4. C. Hamani, and J.N. Nobrega Preclinical studies modeling deep brain stimulation for depression Biol Psychiatry 72 2012 916 923
5. C. Hamani, and Y. Temel Deep brain stimulation for psychiatric disease: Contributions and validity of animal models Sci Transl Med 4 2012 142rv8
6. C. Hamani, M. Diwan, C.E. Macedo, M.L. Brandão, J. Shumake, and F. Gonzalez-Lima et al. Antidepressant-like effects of medial prefrontal cortex deep brain stimulation in rats Biol Psychiatry 67 2010 117 124
7. C. Hamani, D.C. Machado, D.C. Hipólide, F.P. Dubiela, D. Suchecki, and C.E. Macedo 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 71 2012 30 35
8. L. Freedman, T. Insel, and Y. Smith Subcortical projections of area 25 (subgenual cortex) of the macaque monkey J Comp Neurol 421 2000 172 188
9. V. Varga, A. Székely, A. Csillag, T. Sharp, and M. Hajós Evidence for a role of GABA interneurones in the cortical modulation of midbrain 5-hydroxytryptamine neurones Neuroscience 106 2001 783 792
10. V. Varga, B. Kocsis, and T. Sharp Electrophysiological evidence for convergence of inputs from the medial prefrontal cortex and lateral habenula on single neurons in the dorsal raphe nucleus Eur J Neurosci 17 2003 280 286
11. R. Vertes Differential projections of the infralimbic and prelimbic cortex in the rat Synapse 51 2004 32 58
12. P. Celada, M. Puig, J. Casanovas, G. Guillazo, and F. Artigas Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: Involvement of serotonin-1A, GABAA, and glutamate receptors J Neurosci 21 2001 9917 9929
13. M.R. Warden, A. Selimbeyoglu, J.J. Mirzabekov, M. Lo, K.R. Thompson, and S. Kim et al. A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge Nature 492 2012 428 432
14. S. Kumar, S.J. Black, R. Hultman, S.T. Szabo, K.D. DeMaio, and d.u. Jeanette et al. Cortical control of affective networks J Neurosci 33 2013 1116 1129
15. P. Matthews, and P. Harrison A morphometric, immunohistochemical, and in situ hybridization study of the dorsal raphe nucleus in major depression, bipolar disorder, schizophrenia, and suicide J Affect Disord 137 2012 125 134
16. C. Hercher, G. Turecki, and N. Mechawar Through the looking glass: examining neuroanatomical evidence for cellular alterations in major depression J Psychiatr Res 43 2009 947 961
17. M. Budisic, D. Karlovic, Z. Trkanjec, A. Lovrencic-Huzjan, V. Vukovic, J. Bosnjak, and V. Demarin Brainstem raphe lesion in patients with major depressive disorder and in patients with suicidal ideation recorded on transcranial sonography Eur Arch Psychiatry Clin Neurosci 260 2010 203 208
18. I.A. Kerman, R. Bernard, W.E. Bunney, E.G. Jones, A.F. Schatzberg, and R.M. Myers et al. Evidence for transcriptional factor dysregulation in the dorsal raphe nucleus of patients with major depressive disorder Front Neurosci 6 2012 135
19. E. Deneris, and S. Wyler Serotonergic transcriptional networks and potential importance to mental health Nat Neurosci 15 2012 519 527
20. J. Espallergues, S. Teegarden, A. Veerakumar, J. Boulden, C. Challis, and J. Jochems et al. HDAC6 regulates glucocorticoid receptor signaling in serotonin pathways with critical impact on stress resilience J Neurosci 32 2012 4400 4416
21. C. Challis, J. Boulden, A. Veerakumar, J. Espallergues, F. Vassoler, and R. Pierce et al. Raphe GABAergic neurons mediate the acquisition of avoidance after social defeat J Neurosci 33 2013 13978 13988
22. O. Berton, C.A. McClung, R.J. Dileone, V. Krishnan, W. Renthal, and S.J. Russo et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress Science 311 2006 864 868
23. S.A. Golden, H.E. Covington 3rd, O. Berton, and S.J. Russo A standardized protocol for repeated social defeat stress in mice Nature Protocols 6 2011 1183 1191
24. H.E. Covington, M.K. Lobo, I. Maze, V. Vialou, J.M. Hyman, and S. Zaman et al. Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex J Neurosci 30 2010 16082 16090
25. M.J. Agterberg, E.N. Spoelstra, S. van der Wijst, J.H. Brakkee, V.M. Wiegant, and R. Hamelink et al. Evaluation of temperature rise and bonding strength in cements used for permanent head attachments in rats and mice Lab Anim 44 2010 264 270
26. F.M. Vassoler, H.D. Schmidt, M.E. Gerard, K.R. Famous, D.A. Ciraulo, and C. Kornetsky et al. Deep brain stimulation of the nucleus accumbens shell attenuates cocaine priming-induced reinstatement of drug seeking in rats J Neurosci 28 2008 8735 8739
27. C.H. Halpern, A. Tekriwal, J. Santollo, J.G. Keating, J.A. Wolf, D. Daniels, and T.L. Bale Amelioration of binge eating by nucleus accumbens shell deep brain stimulation in mice involves D2 receptor modulation J Neurosci 33 2013 7122 7129
28. F.M. Vassoler, S.L. White, T.J. Hopkins, L.A. Guercio, J. Espallergues, and O. Berton et al. Deep brain stimulation of the nucleus accumbens shell attenuates cocaine reinstatement through local and antidromic activation J Neurosci 33 2013 14446 14454
29. S.M. Falowski, A. Sharan, B.A. Reyes, C. Sikkema, P. Szot, and E.J. van Bockstaele An evaluation of neuroplasticity and behavior after deep brain stimulation of the nucleus accumbens in an animal model of depression Neurosurgery 69 2011 1281 1290
30. C. Schmuckermair, S. Gaburro, A. Sah, R. Landgraf, S.B. Sartori, and N. Singewald Behavioral and neurobiological effects of deep brain stimulation in a mouse model of high anxiety- and depression-like behavior Neuropsychopharmacology 38 2013 1234 1244
31. C. Dournes, S. Beeské, C. Belzung, and G. Griebel Deep brain stimulation in treatment-resistant depression in mice: Comparison with the CRF1 antagonist, SSR125543 Prog Neuropsychopharmacol Biol Psychiatry 40 2013 213 220
32. L.K. Crawford, C.P. Craige, and S.G. Beck Increased intrinsic excitability of lateral wing serotonin neurons of the dorsal raphe: A mechanism for selective activation in stress circuits J Neurophysiol 103 2010 2652 2663
33. L.H. Calizo, A. Akanwa, X. Ma, Y. Pan, J.C. Lemos, and C. Craige et al. Raphe serotonin neurons are not homogenous: electrophysiological, morphological and neurochemical evidence Neuropharmacology 61 2011 524 543
34. L.K. Crawford, S.F. Rahman, and S.G. Beck Social stress alters inhibitory synaptic input to distinct subpopulations of raphe serotonin neurons ACS Chemical Neuroscience 4 2013 200 209
35. D. Rylander, M. Parent, S.S. O'Sullivan, S. Dovero, A.J. Lees, and E. Bezard et al. Maladaptive plasticity of serotonin axon terminals in levodopa-induced dyskinesia Ann Neurol 68 2010 619 628
36. Z. Zhang, J. Kang il, and E. Vaucher Axonal varicosity density as an index of local neuronal interactions PloS One 6 2011 e22543
37. C.J. Wierenga, A. Schuemann, A. Klawiter, T. Bonhoeffer, and C.J. Wierenga Structural plasticity of GABAergic axons is regulated by network activity and GABAA receptor activation Front Neural Circuits 7 2013 113
38. W.B. Hoover, and R.P. Vertes Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat Brain Struct Funct 212 2007 149 179
39. L.K. Crawford, C.P. Craige, and S.G. Beck Glutamatergic input is selectively increased in dorsal raphe subfield 5-HT neurons: Role of morphology, topography and selective innervation Eur J Neurosci 34 2011 1794 1806
40. F.F. De-Miguel, and C. Trueta Synaptic and extrasynaptic secretion of serotonin Cell Mol Neurobiol 25 2005 297 312
41. D.D. Stettler, H. Yamahachi, W. Li, W. Denk, and C.D. Gilbert Axons and synaptic boutons are highly dynamic in adult visual cortex Neuron 49 2006 877 887
42. V. Paola, A. Holtmaat, G. Knott, Song, L. Wilbrecht, P. Caroni, and K. Svoboda Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex Neuron 49 2006 861 875
43. C. Hamani, M. Diwan, S. Isabella, A.M. Lozano, and J.N. Nobrega Effects of different stimulation parameters on the antidepressant-like response of medial prefrontal cortex deep brain stimulation in rats J Psychiatr Res 44 2011 683 687
44. B. Li, J. Piriz, M. Mirrione, C. Chung, C.D. Proulx, and D. Schulz et al. Synaptic potentiation onto habenula neurons in the learned helplessness model of depression Nature 470 2011 535 539
45. V. Krishnan, M. Han, D. Graham, O. Berton, W. Renthal, and S. Russo et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions Cell 131 2007 391 404
46. A. Kalueff, D. Avgustinovich, N. Kudryavtseva, and D. Murphy BDNF in anxiety and depression Science 312 2006 1598 1599 author reply 1598-1599
47. F. Henn Circuits, cells, and synapses: Toward a new target for deep brain stimulation in depression Neuropsychopharmacology 37 2012 307 308
48. E. Montgomery, and J. Gale Mechanisms of action of deep brain stimulation (DBS) Neurosci Biobehav Rev 32 2008 388 407
49. R.A. van Elburg, and A. van Ooyen Impact of dendritic size and dendritic topology on burst firing in pyramidal cells PLoS Comput Biol 6 2010 e1000781
50. O. Prange, T.P. Wong, K. Gerrow, Y.T. Wang, and A. El-Husseini A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin Proc Nat Acad Sci U S A 101 2004 13915 13920
51. M.P. Jankowski, and S.R. Sesack Prefrontal cortical projections to the rat dorsal raphe nucleus: Ultrastructural features and associations with serotonin and γ-aminobutyric acid neurons J Comp Neurol 468 2004 518 529
52. A. Vyas, R. Mitra, B.S. Rao, and S. Chattarji Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons J Neurosci 22 2002 6810 6818
53. G. Paxinos, and K. Franklin The Mouse Brain in Stereotaxic Coordinates 2nd Edition 2001 Academic Press San Diego