High-frequency stimulation of the subthalamic nucleus inhibits the firing of juxtacellular labelled 5-HT-containing neurones

Neuroscience

Volumn 186, Issue , 2011, Pages 135-145

  Hartung, H ^a   Tan, S K H ^b,c,d   Steinbusch, H M W ^b,d   Temel, Y ^b,c,d   Sharp, T ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^d School for Mental Health and Neuroscience   (Netherlands)

Author keywords

5 HT; Deep brain stimulation; Depression; Dorsal raphe nucleus; In vivo electrophysiology; Parkinson's disease

Indexed keywords

BIOTIN; NEUROBIOTIN; SEROTONIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPSY; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; ELECTROPHYSIOLOGY; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; RAT; SEROTONINERGIC NERVE CELL; SUBTHALAMIC NUCLEUS;

ACTION POTENTIALS; ANIMALS; ELECTRIC STIMULATION THERAPY; MALE; MESENCEPHALON; NEURAL INHIBITION; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; SUBTHALAMIC NUCLEUS;

EID: 79957983508     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.04.004     Document Type: Article

References (64)

1. Aghajanian G.K., Wang R.Y. Habenular and other midbrain raphe afferents demonstrated by a modified retrograde tracing technique. Brain Res 1977, 122:229-242.
2. Allers K.A., 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.
3. Appleby B.S., Duggan P.S., Regenberg A., Rabins P.V. Psychiatric and neuropsychiatric adverse events associated with deep brain stimulation: a meta-analysis of ten years' experience. Mov Disord 2007, 22:1722-1728.
4. Baunez C., Humby T., Eagle D.M., Ryan L.J., Dunnett S.B., Robbins T.W. Effects of STN lesions on simple vs choice reaction time tasks in the rat: preserved motor readiness, but impaired response selection. Eur J Neurosci 2001, 13:1609-1616.
5. Baunez C., Nieoullon A., Amalric M. In a rat model of parkinsonism, lesions of the subthalamic nucleus reverse increases of reaction time but induce a dramatic premature responding deficit. J Neurosci 1995, 15:6531-6541.
6. Baunez C., Robbins T.W. Bilateral lesions of the subthalamic nucleus induce multiple deficits in an attentional task in rats. Eur J Neurosci 1997, 9:2086-2099.
7. Bjorvatn B., Fornal C.A., Martin F.J., Metzler C.W., Jacobs B.L. The 5-HT1A receptor antagonist p-MPPI blocks 5-HT1A autoreceptors and increases dorsal raphe unit activity in awake cats. Eur J Pharmacol 1998, 356:167-178.
8. Carlson J.D., Cleary D.R., Cetas J.S., Heinricher M.M., Burchiel K.J. Deep brain stimulation does not silence neurons in subthalamic nucleus in Parkinson's patients. J Neurophysiol 2010, 103:962-967.
9. Carver C.S., Johnson S.L., Joormann J. Serotonergic function, two-mode models of self-regulation, and vulnerability to depression: what depression has in common with impulsive aggression. Psychol Bull 2008, 134:912-943.
10. Chudasama Y., Baunez C., Robbins T.W. Functional disconnection of the medial prefrontal cortex and subthalamic nucleus in attentional performance: evidence for corticosubthalamic interaction. J Neurosci 2003, 23:5477-5485.
11. Cowen P.J. Serotonin and depression: pathophysiological mechanism or marketing myth?. Trends Pharmacol Sci 2008, 29:433-436.
12. Dayan P., Huys Q.J. Serotonin in affective control. Annu Rev Neurosci 2010, 32:95-126.
13. Degos B., Deniau J.M., Thierry A.M., Glowinski J., Pezard L., Maurice N. Neuroleptic-induced catalepsy: electrophysiological mechanisms of functional recovery induced by high-frequency stimulation of the subthalamic nucleus. J Neurosci 2005, 25:7687-7696.
14. Degos B., Deniau J.M., Le Cam J., Mailly P., Maurice N. Evidence for a direct subthalamo-cortical loop circuit in the rat. Eur J Neurosci 2008, 27:2599-2610.
15. Desbonnet L., Temel Y., Visser-Vandewalle V., Blokland A., Hornikx V., Steinbusch H.W. Premature responding following bilateral stimulation of the rat subthalamic nucleus is amplitude and frequency dependent. Brain Res 2004, 1008:198-204.
16. Fineberg N.A., Potenza M.N., Chamberlain S.R., Berlin H.A., Menzies L., Bechara A., Sahakian B.J., Robbins T.W., Bullmore E.T., Hollander E. Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review. Neuropsychopharmacology 2010, 35:591-604.
17. Frank M.J., Samanta J., Moustafa A.A., Sherman S.J. Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science 2007, 318:1309-1312.
18. Fuentealba P., Klausberger T., Karayannis T., Suen W.Y., Huck J., Tomioka R., Rockland K., Capogna M., Studer M., Morales M., Somogyi P. Expression of COUP-TFII nuclear receptor in restricted GABAergic neuronal populations in the adult rat hippocampus. J Neurosci 2010, 30:1595-1609.
19. Groenewegen H.J., Berendse H.W. Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J Comp Neurol 1990, 294:607-622.
20. Groenewegen H.J., Berendse H.W., Haber S.N. Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents. Neuroscience 1993, 57:113-142.
21. Gubellini P., Salin P., Kerkerian-Le Goff L., Baunez C. Deep brain stimulation in neurological diseases and experimental models: from molecule to complex behavior. Prog Neurobiol 2009, 89:79-123.
22. Hajós M., Allers K.A., Jennings K., Sharp T., Charette G., Sik A., Kocsis B. Neurochemical identification of stereotypic burst-firing neurons in the rat dorsal raphe nucleus using juxtacellular labelling methods. Eur J Neurosci 2007, 25:119-126.
23. Hajós M., Richards C.D., Szekely A.D., 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.
24. Hariz M.I., Rehncrona S., Quinn N.P., Speelman J.D., Wensing C. Multicenter study on deep brain stimulation in Parkinson's disease: an independent assessment of reported adverse events at 4 years. Mov Disord 2008, 23:416-421.
25. Hartwich K., Pollak T., Klausberger T. Distinct firing patterns of identified basket and dendrite-targeting interneurons in the prefrontal cortex during hippocampal theta and local spindle oscillations. J Neurosci 2009, 29:9563-9574.
26. Inokawa H., Yamada H., Matsumoto N., Muranishi M., Kimura M. Juxtacellular labeling of tonically active neurons and phasically active neurons in the rat striatum. Neuroscience 2010, 168:395-404.
27. Jacobs B.L., Heym J., Rasmussen K. Raphe neurons: firing rate correlates with size of drug response. Eur J Pharmacol 1983, 90:275-278.
28. Kalen P., Skagerberg G., Lindvall O. Projections from the ventral tegmental area and mesencephalic raphe to the dorsal raphe nucleus in the rat. Evidence for a minor dopaminergic component. Exp Brain Res 1988, 73:69-77.
29. Kirby L.G., Pernar L., Valentino R.J., Beck S.G. Distinguishing characteristics of serotonin and non-serotonin-containing cells in the dorsal raphe nucleus: electrophysiological and immunohistochemical studies. Neuroscience 2003, 116:669-683.
30. Kirouac G.J., Li S., Mabrouk G. GABAergic projection from the ventral tegmental area and substantia nigra to the periaqueductal gray region and the dorsal raphe nucleus. J Comp Neurol 2004, 469:170-184.
31. Kocsis B., Varga V., Dahan L., Sik A. Serotonergic neuron diversity: identification of raphe neurons with discharges time-locked to the hippocampal theta rhythm. Proc Natl Acad Sci U S A 2006, 103:1059-1064.
32. Lacey C.J., Bolam J.P., Magill P.J. Novel and distinct operational principles of intralaminar thalamic neurons and their striatal projections. J Neurosci 2007, 27:4374-4384.
33. Lee K.H., Roberts D.W., Kim U. Effect of high-frequency stimulation of the subthalamic nucleus on subthalamic neurons: an intracellular study. Stereotact Funct Neurosurg 2003, 80:32-36.
34. Lee K.H., Blaha C.D., Harris B.T., Cooper S., Hitti F.L., Leiter J.C., Roberts D.W., Kim U. Dopamine efflux in the rat striatum evoked by electrical stimulation of the subthalamic nucleus: potential mechanism of action in Parkinson's disease. Eur J Neurosci 2006, 23:1005-1014.
35. Li X.H., Wang J.Y., Gao G., Chang J.Y., Woodward D.J., Luo F. High-frequency stimulation of the subthalamic nucleus restores neural and behavioral functions during reaction time task in a rat model of Parkinson's disease. J Neurosci Res 2010, 88:1510-1521.
36. Mann J.J. Neurobiology of suicidal behaviour. Nat Rev Neurosci 2003, 4:819-828.
37. Maurice N., Thierry A.M., Glowinski J., Deniau J.M. Spontaneous and evoked activity of substantia nigra pars reticulata neurons during high-frequency stimulation of the subthalamic nucleus. J Neurosci 2003, 23:9929-9936.
38. Michelsen K.A., Schmitz C., Steinbusch H.W. The dorsal raphe nucleus-from silver stainings to a role in depression. Brain Res Rev 2007, 55:329-342.
39. 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.
40. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press Ltd, London.
41. Peyron C., Petit J.M., Rampon C., Jouvet M., Luppi P.H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 1998, 82:443-468.
42. Phillips J.M., Brown V.J. Reaction time performance following unilateral striatal dopamine depletion and lesions of the subthalamic nucleus in the rat. Eur J Neurosci 1999, 11:1003-1010.
43. Phillips J.M., Brown V.J. Anticipatory errors after unilateral lesions of the subthalamic nucleus in the rat: evidence for a failure of response inhibition. Behav Neurosci 2000, 114:150-157.
44. Pinault D. A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or neurobiotin. J Neurosci Methods 1996, 65:113.
45. Rodrigues A.M., Rosas M.J., Gago M.F., Sousa C., Fonseca R., Linhares P., Basto M.A., Sousa G., Garrett C., Vaz R. Suicide attempts after subthalamic nucleus stimulation for Parkinson's disease. Eur Neurol 2010, 63:176-179.
46. Ros H., Magill P.J., Moss J., Bolam J.P., Mena-Segovia J. Distinct types of non-cholinergic pedunculopontine neurons are differentially modulated during global brain states. Neuroscience 2010, 170:78-91.
47. Schweimer J.V., Ungless M.A. Phasic responses in dorsal raphe serotonin neurons to noxious stimuli. Neuroscience 2010, 171:1209-1215.
48. Smith K.A., Fairburn C.G., Cowen P.J. Relapse of depression after rapid depletion of tryptophan. Lancet 1997, 349:915-919.
49. Tai C.H., Boraud T., Bezard E., Bioulac B., Gross C., Benazzouz A. Electrophysiological and metabolic evidence that high-frequency stimulation of the subthalamic nucleus bridles neuronal activity in the subthalamic nucleus and the substantia nigra reticulata. FASEB J 2003, 17:1820-1830.
50. Tan S, Hartung H, Visser-Vandewalle V, Steinbusch H, Temel Y, Sharp T (2010a) High-frequency stimulation of the subthalamic nucleus inhibits the firing of juxtacellular labelled 5-HT-containing neurons and decreases 5-HT release in vivo. Society for Neuroscience, San Diego meeting, Abstract 459.18.
51. Tan S., Vlamings R., Lim L., Sesia T., Janssen M.L., Steinbusch H.W., Visser-Vandewalle V., Temel Y. Experimental deep brain stimulation in animal models. Neurosurgery 2010, 67:1073-1079.
52. Temel Y., Boothman L.J., Blokland A., Magill P.J., Steinbusch H.W., Visser-Vandewalle V., Sharp T. Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc Natl Acad Sci U S A 2007, 104:17087-17092.
53. Temel Y., Kessels A., Tan S., Topdag A., Boon P., Visser-Vandewalle V. Behavioural changes after bilateral subthalamic stimulation in advanced Parkinson disease: a systematic review. Parkinsonism Relat Disord 2006, 12:265-272.
54. Temel Y., Visser-Vandewalle V., Aendekerk B., Rutten B., Tan S., Scholtissen B., Schmitz C., Blokland A., Steinbusch H.W. Acute and separate modulation of motor and cognitive performance in parkinsonian rats by bilateral stimulation of the subthalamic nucleus. Exp Neurol 2005, 193:43-52.
55. Temel Y., Visser-Vandewalle V., Kaplan S., Kozan R., Daemen M.A., Blokland A., Schmitz C., Steinbusch H.W. Protection of nigral cell death by bilateral subthalamic nucleus stimulation. Brain Res 2006, 1120:100-105.
56. Troster A.I., Fields J.A., Wilkinson S., Pahwa R., Koller W.C., Lyons K.E. Effect of motor improvement on quality of life following subthalamic stimulation is mediated by changes in depressive symptomatology. Stereotact Funct Neurosurg 2003, 80:43-47.
57. Varga V., Kocsis B., Sharp T. 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 2003, 17:280-286.
58. Varga V., Szekely A.D., Csillag A., Sharp T., Hajós M. Evidence for a role of GABA interneurones in the cortical modulation of midbrain 5-hydroxytryptamine neurones. Neuroscience 2001, 106:783-792.
59. Vlamings R., Visser-Vandewalle V., Koopmans G., Joosten E.A., Kozan R., Kaplan S., Steinbusch H.W., Temel Y. High frequency stimulation of the subthalamic nucleus improves speed of locomotion but impairs forelimb movement in Parkinsonian rats. Neuroscience 2007, 148:815-823.
60. Vlamings R., Visser-Vandewalle V., Kozan R., Kaplan S., Steinbusch H.W., Temel Y. Bilateral high frequency stimulation of the subthalamic nucleus normalizes COX activity in the substantia nigra of Parkinsonian rats. Brain Res 2009, 1288:143-148.
61. Voon V., Krack P., Lang A.E., Lozano A.M., Dujardin K., Schupbach M., D'Ambrosia J., Thobois S., Tamma F., Herzog J., Speelman J.D., Samanta J., Kubu C., Rossignol H., Poon Y.Y., Saint-Cyr J.A., Ardouin C., Moro E. A multicentre study on suicide outcomes following subthalamic stimulation for Parkinson's disease. Brain 2008, 131:2720-2728.
62. Voon V., Kubu C., Krack P., Houeto J.L., Troster A.I. Deep brain stimulation: neuropsychological and neuropsychiatric issues. Mov Disord 2006, 21(Suppl 14):S305-S327.
63. Weaver F.M., Follett K., Stern M., Hur K., Harris C., Marks W.J., Rothlind J., Sagher O., Reda D., Moy C.S., Pahwa R., Burchiel K., Hogarth P., Lai E.C., Duda J.E., Holloway K., Samii A., Horn S., Bronstein J., Stoner G., Heemskerk J., Huang G.D. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA 2009, 301:63-73.
64. Williams A., Gill S., Varma T., Jenkinson C., Quinn N., Mitchell R., Scott R., Ives N., Rick C., Daniels J., Patel S., Wheatley K. Deep brain stimulation plus best medical therapy versus best medical therapy alone for advanced Parkinson's disease (PD SURG trial): a randomised, open-label trial. Lancet Neurol 2010, 9:581-591.