Deep brain electrophysiological recordings provide clues to the pathophysiology of Tourette syndrome

Neuroscience and Biobehavioral Reviews

Volumn 37, Issue 6, 2013, Pages 1063-1068

  Priori, Alberto ^a,b   Giannicola, Gaia ^a,b   Rosa, Manuela ^a   Marceglia, Sara ^a,c   Servello, Domenico ^d   Sassi, Marco ^d   Porta, Mauro ^d  

^a FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c POLITECNICO DI MILANO   (Italy)

^d IRCCS ISTITUTO ORTOPEDICO GALEAZZI   (Italy)

Author keywords

Adaptive deep brain stimulation; Deep brain stimulation; Local field potentials; Long term recordings; Low frequency; Microrecordings; Movement disorders; Neurophysiology; Neurosurgery; Pathophysiology; Tic; Tourette syndrome

Indexed keywords

BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; GAMMA RHYTHM; GILLES DE LA TOURETTE SYNDROME; GLOBUS PALLIDUS; HIGH FREQUENCY OSCILLATION; HUMAN; LOCAL FIELD POTENTIAL; NERVOUS SYSTEM POTENTIAL; NEUROMODULATION; NEUROPATHOLOGY; NEUROPHYSIOLOGY; NONHUMAN; NUCLEUS ACCUMBENS; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; THALAMUS MIDLINE NUCLEUS; THALAMUS VENTRAL NUCLEUS; ARTICLE; BRAIN; ELECTROPHYSIOLOGY; PATHOLOGY; PHYSIOLOGY;

BRAIN; DEEP BRAIN STIMULATION; ELECTROPHYSIOLOGICAL PHENOMENA; HUMANS; TOURETTE SYNDROME;

EID: 84891896333     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2013.01.011     Document Type: Review

References (87)

1. Ackermans L., Duits A., Temel Y., Winogrodzka A., Peeters F., Beuls E.A., Visser-Vandewalle V. Long-term outcome of thalamic deep brain stimulation in two patients with Tourette syndrome. Journal of Neurology, Neurosurgery and Psychiatry 2010, 81:1068-1072.
2. Ackermans L., Temel Y., Visser-Vandewalle V. Deep brain stimulation in neurological and psychiatric disorders. Deep Brain Stimulation in Tourette's Syndrome 2008, Humana Press, Totowa, NJ, pp. 321-332. D. Tarsy, J.L. Vitek, P.A. Starr (Eds.).
3. Ackermans L., Temel Y., Visser-Vandewalle V. Deep brain stimulation in Tourette's Syndrome. Neurotherapeutics 2008, 5:339-344.
4. Albin R.L., Mink J.W. Recent advances in Tourette syndrome research. Trends in Neurosciences 2006, 29:175-182.
5. Alonso-Frech F., Zamarbide I., Alegre M., Rodriguez-Oroz M.C., Guridi J., Manrique M., Valencia M., Artieda J., Obeso J.A. Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson's disease. Brain 2006, 129:1748-1757.
6. Bevan M.D., Magill P.J., Terman D., Bolam J.P., Wilson C.J. Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends in Neurosciences 2002, 25:525-531.
7. Brown P., Eusebio A. Paradoxes of functional neurosurgery: clues from basal ganglia recordings. Movement Disorders 2008, 23:12-20. quiz 158.
8. Brown P., Williams D. Basal ganglia local field potential activity: character and functional significance in the human. Clinical Neurophysiology 2005, 116:2510-2519.
9. Burdick A., Foote K.D., Goodman W., Ward H.E., Ricciuti N., Murphy T., Haq I., Okun M.S. Lack of benefit of accumbens/capsular deep brain stimulation in a patient with both tics and obsessive-compulsive disorder. Neurocase 2010, 16:321-330.
10. Cannon E., Silburn P., Coyne T., O'Maley K., Crawford J.D., Sachdev P.S. Deep brain stimulation of anteromedial globus pallidus interna for severe Tourette's syndrome. American Journal of Psychiatry 2012, 169:860-866.
11. Cordella R., Carella F., Franzini A., Marras C., Villani F., Messina G., Tringali G., Broggi G. Intraoperative microrecordings in the posterior hypothalamus of anaesthetized humans with aggressive behaviour. Neurological Sciences 2010, 31:183-188.
12. de Koning P.P., Figee M., van den Munckhof P., Schuurman P.R., Denys D. Current status of deep brain stimulation for obsessive-compulsive disorder: a clinical review of different targets. Current Psychiatry Reports 2011, 13:274-282.
13. Diederich N.J., Kalteis K., Stamenkovic M., Pieri V., Alesch F. Efficient internal pallidal stimulation in Gilles de la Tourette syndrome: a case report. Movement Disorders 2005, 20:1496-1499.
14. Draganski B., Martino D., Cavanna A.E., Hutton C., Orth M., Robertson M.M., Critchley H.D., Frackowiak R.S. Multispectral brain morphometry in Tourette syndrome persisting into adulthood. Brain 2010, 133:3661-3675.
15. Eusebio A., Thevathasan W., Doyle Gaynor L., Pogosyan A., Bye E., Foltynie T., Zrinzo L., Ashkan K., Aziz T., Brown P. Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients. Journal of Neurology, Neurosurgery and Psychiatry 2010, 82:569-573.
16. Foffani G., Ardolino G., Meda B., Egidi M., Rampini P., Caputo E., Baselli G., Priori A. Altered subthalamo-pallidal synchronisation in parkinsonian dyskinesias. Journal of Neurology, Neurosurgery and Psychiatry 2005, 76:426-428.
17. Francois C., Percheron G., Parent A., Sadikot A.F., Fenelon G., Yelnik J. Topography of the projection from the central complex of the thalamus to the sensorimotor striatal territory in monkeys. Journal of Comparative Neurology 1991, 305:17-34.
18. Francois C., Percheron G., Yelnik J., Tande D. A topographic study of the course of nigral axons and of the distribution of pallidal axonal endings in the centre median-parafascicular complex of macaques. Brain Research 1988, 473:181-186.
19. Fumagalli M., Priori A. Functional and clinical neuroanatomy of morality. Brain 2012, 135:2006-2021.
20. Gatev P., Darbin O., Wichmann T. Oscillations in the basal ganglia under normal conditions and in movement disorders. Movement Disorders 2006, 21:1566-1577.
21. Giannicola, G., Ciocca, M., Scelzo, E., Rosa, M., Servello, D., Porta, M., Barbieri, S., Priori, A., in press. In: Vitek, J.L. (Ed.), Deep Brain Stimulation: Technology and Applications. Chapter 10: DBS and Tics, doi:10.2217/EBO.12.511.
22. Giannicola G., Marceglia S., Rossi L., Mrakic-Sposta S., Rampini P., Tamma F., Cogiamanian F., Barbieri S., Priori A. The effects of levodopa and ongoing deep brain stimulation on subthalamic beta oscillations in Parkinson's disease. Experimental Neurology 2010, 226:120-127.
23. Giannicola G., Priori A. Stormy weather in the human basal ganglia. Clinical Neurophysiology 2012, doi:10.1016/j.clinph.2012.09.012.
24. Giannicola G., Rosa M., Marceglia S., Scelzo E., Rossi L., Servello D., Menghetti C., Pacchetti C., Zangaglia R., Locatelli M., Caputo E., Cogiamanian F., Ardolino G., Barbieri S., Priori A. The effects of levodopa and deep brain stimulation on subthalamic local field low-frequency oscillations in Parkinson's disease. Neurosignals 2012, doi:10.1159/000336543.
25. Giannicola G., Rosa M., Servello D., Menghetti C., Carrabba G., Pacchetti C., Zangaglia R., Cogiamanian F., Scelzo E., Marceglia S., Rossi L., Priori A. Subthalamic local field potentials after seven-years deep brain stimulation in Parkinson's disease. Experimental Neurology 2012, 237:312-317.
26. Goetz C.G., Tanner C.M., Wilson R.S., Carroll V.S., Como P.G., Shannon K.M. Clonidine and Gilles de la Tourette's syndrome: double-blind study using objective rating methods. Annals of Neurology 1987, 21:307-310.
27. Groenewegen H.J., van den Heuvel O.A., Cath D.C., Voorn P., Veltman D.J. Does an imbalance between the dorsal and ventral striatopallidal systems play a role in Tourette's syndrome? A neuronal circuit approach. Brain and Development 2003, 25(Suppl. 1):S3-S14.
28. Hodaie M., Cordella R., Lozano A.M., Wennberg R., Dostrovsky J.O. Bursting activity of neurons in the human anterior thalamic nucleus. Brain Research 2006, 1115:1-8.
29. Houeto J.L., Karachi C., Mallet L., Pillon B., Yelnik J., Mesnage V., Welter M.L., Navarro S., Pelissolo A., Damier P., Pidoux B., Dormont D., Cornu P., Agid Y. Tourette's syndrome and deep brain stimulation. Journal of Neurology, Neurosurgery and Psychiatry 2005, 76:992-995.
30. Jeanmonod D., Magnin M., Morel A. Low-threshold calcium spike bursts in the human thalamus. Common physiopathology for sensory, motor and limbic positive symptoms. Brain 1996, 119(Pt 2):363-375.
31. Karp B.I., Porter S., Toro C., Hallett M. Simple motor tics may be preceded by a premotor potential. Journal of Neurology, Neurosurgery and Psychiatry 1996, 61:103-106.
32. Kurlan R. Clinical practice. Tourette's syndrome. New England Journal of Medicine 2010, 363:2332-2338.
33. Kwak C.H., Hanna P.A., Jankovic J. Botulinum toxin in the treatment of tics. Archives of Neurology 2000, 57:1190-1193.
34. Leckman J.F., Hardin M.T., Riddle M.A., Stevenson J., Ort S.I., Cohen D.J. Clonidine treatment of Gilles de la Tourette's syndrome. Archives of General Psychiatry 1991, 48:324-328.
35. Levy R., Ashby P., Hutchison W.D., Lang A.E., Lozano A.M., Dostrovsky J.O. Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease. Brain 2002, 125:1196-1209.
36. Llinas R., Urbano F.J., Leznik E., Ramirez R.R., van Marle H.J. Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends in Neurosciences 2005, 28:325-333.
37. Maling N., Hashemiyoon R., Foote K.D., Okun M.S., Sanchez J.C. Increased thalamic gamma band activity correlates with symptom relief following deep brain stimulation in humans with Tourette's syndrome. PLOS ONE 2012, 7:e44215.
38. Marceglia S., Bianchi A.M., Baselli G., Foffani G., Cogiamanian F., Modugno N., Mrakic-Sposta S., Priori A., Cerutti S. Interaction between rhythms in the human basal ganglia: application of bispectral analysis to local field potentials. IEEE Transactions on Neural Systems and Rehabilitation Engineering 2007, 15:483-492.
39. Marceglia S., Fumagalli M., Priori A. What neurophysiological recordings tell us about cognitive and behavioral functions of the human subthalamic nucleus. Expert Reviews in Neurotherapy 2011, 11:139-149.
40. Marceglia S., Servello D., Foffani G., Porta M., Sassi M., Mrakic-Sposta S., Rosa M., Barbieri S., Priori A. Thalamic single-unit and local field potential activity in Tourette syndrome. Movement Disorders 2010, 25:300-308.
41. Martinez-Fernandez R., Zrinzo L., Aviles-Olmos I., Hariz M., Martinez-Torres I., Joyce E., Jahanshahi M., Limousin P., Foltynie T. Deep brain stimulation for Gilles de la Tourette syndrome: a case series targeting subregions of the globus pallidus internus. Movement Disorders 2011, 26:1922-1930.
42. Martinez-Torres I., Hariz M.I., Zrinzo L., Foltynie T., Limousin P. Improvement of tics after subthalamic nucleus deep brain stimulation. Neurology 2009, 72:1787-1789.
43. McCracken C.B., Grace A.A. High-frequency deep brain stimulation of the nucleus accumbens region suppresses neuronal activity and selectively modulates afferent drive in rat orbitofrontal cortex in vivo. Journal of Neuroscience 2007, 27:12601-12610.
44. Mink J.W. Basal ganglia dysfunction in Tourette's syndrome: a new hypothesis. Pediatric Neurology 2001, 25:190-198.
45. Mink J.W. Neurobiology of basal ganglia circuits in Tourette syndrome: faulty inhibition of unwanted motor patterns?. Advances in Neurology 2001, 85:113-122.
46. Mink J.W. The Basal Ganglia and involuntary movements: impaired inhibition of competing motor patterns. Archives of Neurology 2003, 60:1365-1368.
47. Mrakic-Sposta S., Marceglia S., Egidi M., Carrabba G., Rampini P., Locatelli M., Foffani G., Accolla E., Cogiamanian F., Tamma F., Barbieri S., Priori A. Extracellular spike microrecordings from the subthalamic area in Parkinson's disease. Journal of Clinical Neuroscience 2008, 15:559-567.
48. Muller-Vahl K.R., Cath D.C., Cavanna A.E., Dehning S., Porta M., Robertson M.M., Visser-Vandewalle V. European clinical guidelines for Tourette syndrome and other tic disorders. Part IV: deep brain stimulation. European Child and Adolescent Psychiatry 2011, 20:209-217.
49. Neuner I., Halfter S., Wollenweber F., Podoll K., Schneider F. Nucleus accumbens deep brain stimulation did not prevent suicide attempt in Tourette syndrome. Biological Psychiatry 2010, 68:e19-e20.
50. Obeso J.A., Rothwell J.C., Marsden C.D. Simple tics in Gilles de la Tourette's syndrome are not prefaced by a normal premovement EEG potential. Journal of Neurology, Neurosurgery and Psychiatry 1981, 44:735-738.
51. Okun M.S., Foote K.D., Wu S.S., Ward H.E., Bowers D., Rodriguez R.L., Malaty I.A., Goodman W.K., Gilbert D.M., Walker H.C., Mink J.W., Merritt S., Morishita T., Sanchez J.C. A trial of scheduled deep brain stimulation for Tourette syndrome: moving away from continuous deep brain stimulation paradigms. Archives of Neurology 2012, doi:10.1001/jamaneurol.2013.580.
52. Porta M., Sassi M., Cavallazzi M., Fornari M., Brambilla A., Servello D. Tourette's syndrome and role of tetrabenazine: review and personal experience. Clinical Drug Investigations 2008, 28:443-459.
53. Porta M., Sassi M., Menghetti C., Servello D. The need for a proper definition of a treatment refractoriness in Tourette syndrome. Frontier Integrative Neuroscience 2011, 5:22.
54. Porta M., Sassi M., Servello D. Tourette Syndrome. Chapter 27: Surgical treatment of Tourette Syndrome 2012, Oxford University Press, USA. D. Martino, J.F. Leckman (Eds.).
55. Porta M., Servello D., Zanaboni C., Anasetti F., Menghetti C., Sassi M., Robertson M.M. Deep brain stimulation for treatment of refractory Tourette syndrome: long-term follow-up. Acta Neurochirurgica 2012, 154:2029-2041.
56. Pringsheim T., Marras C. Pimozide for tics in Tourette's syndrome. Cochrane Database System Review 2009, CD006996.
57. Priori A., Egidi M., Pesenti A., Rohr M., Rampini P., Locatelli M., Tamma F., Caputo E., Chiesa V., Barbieri S. Do intraoperative microrecordings improve subthalamic nucleus targeting in stereotactic neurosurgery for Parkinson's disease. Journal of Neurosurgical Sciences 2003, 47:56-60.
58. Priori A., Foffani G., Pesenti A., Tamma F., Bianchi A.M., Pellegrini M., Locatelli M., Moxon K.A., Villani R.M. Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease. Experimental Neurology 2004, 189:369-379.
59. Priori, A., Foffani, G., Rossi, L., 2005. Apparatus for treating neurological disorders by means of adaptive electro-stimulation retroacted by biopotentials. EU Patent Office, n. 1940508.
60. Priori, A., Foffani, G., Rossi, L., 2005. Apparatus for treating neurological disorders by means of adaptive electro-stimulation retroacted by biopotentials. US Patent Office, n. 8078281.
61. Priori A., Foffani G., Rossi L., Marceglia S. Adaptive deep brain stimulation (aDBS) controlled by local field potential oscillations. Experimental Neurology 2012, doi:10.1016/j.expneurol.2012.09.013.
62. Rosa M., Franzini A., Giannicola G., Messina G., Altamura A.C., Priori A. Hypothalamic oscillations in human pathological aggressiveness. Biological Psychiatry 2012, 72:e33-e35.
63. Rosa M., Giannicola G., Marceglia S., Fumagalli M., Barbieri S., Priori A. Neurophysiology of deep brain stimulation. International Review of Neurobiology 2012, 107:23-55.
64. Rosa M., Giannicola G., Servello D., Marceglia S., Pacchetti C., Porta M., Sassi M., Scelzo E., Barbieri S., Priori A. Subthalamic local field beta oscillations during ongoing deep brain stimulation in Parkinson's disease in hyperacute and chronic phases. Neuro-signals 2011, 19:151-162.
65. Rossi L., Marceglia S., Foffani G., Cogiamanian F., Tamma F., Rampini P., Barbieri S., Bracchi F., Priori A. Subthalamic local field potential oscillations during ongoing deep brain stimulation in Parkinson's disease. Brain Research Bulletin 2008, 76:512-521.
66. Rubino D., Robbins K.A., Hatsopoulos N.G. Propagating waves mediate information transfer in the motor cortex. Nature Neuroscience 2006, 9:1549-1557.
67. Saka E., Graybiel A.M. Pathophysiology of Tourette's syndrome: striatal pathways revisited. Brain and Development 2003, 25(Suppl. 1):S15L 19.
68. Sallee F.R., Nesbitt L., Jackson C., Sine L., Sethuraman G. Relative efficacy of haloperidol and pimozide in children and adolescents with Tourette's disorder. American Journal of Psychiatry 1997, 154:1057-1062.
69. Scahill L., Chappell P.B., Kim Y.S., Schultz R.T., Katsovich L., Shepherd E., Arnsten A.F., Cohen D.J., Leckman J.F. A placebo-controlled study of guanfacine in the treatment of children with tic disorders and attention deficit hyperactivity disorder. American Journal of Psychiatry 2001, 158:1067-1074.
70. Segawa M. Neurophysiology of Tourette's syndrome: pathophysiological considerations. Brain and Development 2003, 25(Suppl. 1):S62L 69.
71. Servello D., Sassi M., Brambilla A., Defendi S., Porta M. Long-term, post-deep brain stimulation management of a series of 36 patients affected with refractory Gilles de La Tourette syndrome. Neuromodulation 2010, 13:187-194.
72. Silberstein P., Kuhn A.A., Kupsch A., Trottenberg T., Krauss J.K., Wohrle J.C., Mazzone P., Insola A., Di Lazzaro V., Oliviero A., Aziz T., Brown P. Patterning of globus pallidus local field potentials differs between Parkinson's disease and dystonia. Brain 2003, 126:2597-2608.
73. Simpson D.M., Blitzer A., Brashear A., Comella C., Dubinsky R., Hallett M., Jankovic J., Karp B., Ludlow C.L., Miyasaki J.M., Naumann M., So Y. Assessment: botulinum neurotoxin for the treatment of movement disorders (an evidence-based review): report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 2008, 70:1699-1706.
74. Terman D., Rubin J.E., Yew A.C., Wilson C.J. Activity patterns in a model for the subthalamopallidal network of the basal ganglia. Journal of Neuroscience 2002, 22:2963-2976.
75. Verdellen C., van de Griendt J., Hartmann A., Murphy T. European clinical guidelines for Tourette syndrome and other tic disorders. Part III: behavioural and psychosocial interventions. European Child and Adolescent Psychiatry 2011, 20:197-207.
76. Vilela, F.O., Ragazzo, P., Souza, J., Silva, D., Oliveira, P., Ribeiro, T., 2010 Bilateral GPe-DBS for Tourette syndrome: a double-blind prospective controlled study of seven patients (abstract). In: Abstract book of the ASSFN (American Society for Stereotactic and Functional Neurosurgery), 2010 biennial meeting. Bridging the Future of Neurosurgery, New York.
77. Visser-Vandewalle V. DBS in Tourette syndrome: rationale, current status and future prospects. Acta Neurochirurgica Supplementum 2007, 97:215-222.
78. Visser-Vandewalle V., Ackermans L., van der Linden C., Temel Y., Tijssen M.A., Schruers K.R., Nederveen P., Kleijer M., Boon P., Weber W., Cath D. Deep brain stimulation in Gilles de la Tourette's syndrome. Neurosurgery 2006, 58:E590.
79. Visser-Vandewalle V., Temel Y., Boon P., Vreeling F., Colle H., Hoogland G., Groenewegen H.J., van der Linden C. Chronic bilateral thalamic stimulation: a new therapeutic approach in intractable Tourette syndrome. Report of three cases. Journal of Neurosurgery 2003, 99:1094-1100.
80. Vitek J.L., Chockkan V., Zhang J.Y., Kaneoke Y., Evatt M., DeLong M.R., Triche S., Mewes K., Hashimoto T., Bakay R.A. Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus. Annals of Neurology 1999, 46:22-35.
81. Welter M.L., Mallet L., Houeto J.L., Karachi C., Czernecki V., Cornu P., Navarro S., Pidoux B., Dormont D., Bardinet E., Yelnik J., Damier P., Agid Y. Internal pallidal and thalamic stimulation in patients with Tourette syndrome. Archives of Neurology 2008, 65:952-957.
82. Wilke M., Logothetis N.K., Leopold D.A. Local field potential reflects perceptual suppression in monkey visual cortex. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:17507-17512.
83. Wingeier B., Tcheng T., Koop M.M., Hill B.C., Heit G., Bronte-Stewart H.M. Intra-operative STN DBS attenuates the prominent beta rhythm in the STN in Parkinson's disease. Experimental Neurology 2006, 197:244-251.
84. Worbe Y., Malherbe C., Hartmann A., Pelegrini-Issac M., Messe A., Vidailhet M., Lehericy S., Benali H. Functional immaturity of cortico-basal ganglia networks in Gilles de la Tourette syndrome. Brain 2012, 135:1937-1946.
85. Zabek M., Sobstyl M., Koziara H., Dzierzecki S. Deep brain stimulation of the right nucleus accumbens in a patient with Tourette syndrome. Case report. Neurologia i Neurochirurgia Polska 2008, 42:554-559.
86. Zhuang P., Hallett M., Zhang X., Li J., Zhang Y., Li Y. Neuronal activity in the globus pallidus internus in patients with tics. Journal of Neurology, Neurosurgery and Psychiatry 2009, 80:1075-1081.
87. Zhuang P., Li Y., Hallett M. Neuronal activity in the basal ganglia and thalamus in patients with dystonia. Clinical Neurophysiology 2004, 115:2542-2557.