Improved sensory gating of urinary bladder afferents in Parkinson's disease following subthalamic stimulation

Brain

Volumn 131, Issue 1, 2008, Pages 132-145

  Herzog, Jan ^a   Weiss, Peter H ^b,c   Assmus, Ann ^b,c   Wefer, Björn ^a   Seif, Christoph ^a   Braun, Peter M ^a   Pinsker, Marcus O ^a   Herzog, Hans ^b   Volkmann, Jens ^a   Deuschl, Günther ^a   Fink, Gereon R ^b,c,d  

^a UNIVERSITY OF KIEL   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c Brain Imaging Center West   (Germany)

^d UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

Author keywords

Deep brain stimulation; Periaqueductal grey; PET; Subthalamic nucleus; Visceral sensory processing

Indexed keywords

AMANTADINE; CABERGOLINE; DOPAMINE RECEPTOR STIMULATING AGENT; LEVODOPA; PRAMIPEXOLE; ROPINIROLE;

ADULT; AGED; ARTICLE; BLADDER; BRAIN BLOOD FLOW; BRAIN DEPTH STIMULATION; CEREBELLUM; CLINICAL ARTICLE; FEMALE; FRONTAL CORTEX; HUMAN; INSULA; MALE; MEASUREMENT; MODULATION; PARKINSON DISEASE; PATHOPHYSIOLOGY; PERIAQUEDUCTAL GRAY MATTER; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REGRESSION ANALYSIS; SENSORY ANALYSIS; SUBTHALAMIC NUCLEUS; THALAMUS POSTERIOR NUCLEUS;

EID: 37549006298     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awm254     Document Type: Article

References (102)

1. Abbruzzese G, Berardelli A. Sensorimotor integration in movement disorders. Mov Disord 2003; 18: 231-40.
2. Allen GV, Saper CB, Hurley KM, Cechetto DF. Organization of visceral and limbic connections in the insular cortex of the rat. J Comp Neurol 1991; 311: 1-16.
3. Andrew J, Nathan PW. Lesions on the anterior frontal lobes and disturbances of micturition and defaecation. Brain 1964; 87: 233-62.
4. Araki I, Kitahara M, Oida T, Kuno S. Voiding dysfunction and Parkinson's disease: urodynamic abnormalities and urinary symptoms. J Urol 2000; 164: 1640-3.
5. Araki I, Kuno S. Assessment of voiding dysfunction in Parkinson's disease by the international prostate symptom score. J Neurol Neurosurg Psychiatry 2000; 68: 429-33.
6. Athwal BS, Berkley KJ, Hussain I, Brennan A, Craggs M, Sakakibara R, et al. Brain responses to changes in bladder volume and urge to void in healthy men. Brain 2001; 124: 369-77.
7. Aziz Q, Thompson DG, Ng VW, Hamdy S, Sarkar S, Brammer MJ, et al. Cortical processing of human somatic and visceral sensation. J Neurosci 2000; 20: 2657-63.
8. Bandini F, Pierantozzi M, Bodis-Wollner I. Parkinson's disease changes the balance of onset and offset visual responses: an evoked potential study. Clin Neurophysiol 2001; 112: 976-83.
9. Blok BF. Brain control of the lower urinary tract. Scand J Urol Nephrol Suppl 2002a; 210: 11-5.
10. Blok BF. Central pathways controlling micturition and urinary continence. Urology 2002b; 59: 13-7.
11. Blok BF, De Weerd H, Holstege G. Ultrastructural evidence for a paucity of projections from the lumbosacral cord to the pontine micturition center or M-region in the cat: a new concept for the organization of the micturition reflex with the periaqueductal gray as central relay. J Comp Neurol 1995; 359: 300-9.
12. Blok BF, Sturms LM, Holstege G. Brain activation during micturition in women. Brain 1998; 121 (Pt 11): 2033-42.
13. Blok BF, Willemsen AT, Holstege G. A PET study on brain control of micturition in humans. Brain 1997; 120 (Pt 1): 111-21.
14. Blomqvist A, Zhang ET, Craig AD. Cytoarchitectonic and immunohistochemical characterization of a specific pain and temperature relay, the posterior portion of the ventral medial nucleus, in the human thalamus. Brain 2000; 123 (Pt 3): 601-19.
15. Boecker H, Ceballos-Baumann A, Bartenstein P, Weindl A, Siebner HR, Fassbender T, et al. Sensory processing in Parkinson's and Huntington's disease: investigations with 3D H(2)(15)O-PET. Brain 1999; 122 (Pt 9): 1651-65.
16. Bonnet AM, Pichon J, Vidailhet M, Gouider-Khouja N, Robain G, Perrigot M, et al. Urinary disturbances in striatonigral degeneration and Parkinson's disease: clinical and urodynamic aspects. Mov Disord 1997; 12: 509-13.
17. Bradley WE, Teague CT. Cerebellar influence on the micturition reflex. Exp Neurol 1969; 23: 399-411.
18. Bragin EO, Yeliseeva ZV, Vasilenko GF, Meizerov EE, Chuvin BT, Durinyan RA. Cortical projections to the periaqueductal grey in the cat: a retrograde horseradish peroxidase study. Neurosci Lett 1984; 51: 271-5.
19. Bruggemann J, Vahle-Hinz C, Kniffki KD. Projections from the pelvic nerve to the periphery of the cat's thalamic ventral posterolateral nucleus and adjacent regions of the posterior complex. J Neurophysiol 1994; 72: 2237-45.
20. Brusa L, Petta F, Pisani A, Moschella V, Iani C, Stanzione P, et al. Acute vs chronic effects of l-dopa on bladder function in patients with mild Parkinson disease. Neurology 2007; 68: 1455-9.
21. Campos-Sousa RN, Quagliato E, da Silva BB, de Carvalho RM Jr, Riberio SC, de Carvalho DF. Urinary symptoms in Parkinson's disease: prevalence and associated factors. Arq Neuropsiquiatr 2003; 61: 359-63.
22. Carrive P. The periaqueductal gray and defensive behavior: functional representation and neuronal organization. Behav Brain Res 1993; 58: 27-47.
23. Carstens E, Yokota T. Viscerosomatic convergence and responses to intestinal distension of neurons at the junction of midbrain and posterior thalamus in the cat. Exp Neurol 1980; 70: 392-402.
24. Ceballos-Baumann AO, Boecker H, Bartenstein P, von Falkenhayn I, Riescher H, Conrad B, et al. A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch Neurol 1999; 56: 997-1003.
25. Chandler MJ, Hobbs SF, Fu QG, Kenshalo DR Jr, Blair RW, Foreman RD. Responses of neurons in ventroposterolateral nucleus of primate thalamus to urinary bladder distension. Brain Res 1992; 571: 26-34.
26. Clasca F, Llamas A, Reinoso-Suarez F. Insular cortex and neighboring fields in the cat: a redefinition based on cortical microarchitecture and connections with the thalamus. J Comp Neurol 1997; 384: 456-82.
27. Craig AD, Bushnell MC, Zhang ET, Blomqvist A. A thalamic nucleus specific for pain and temperature sensation. Nature 1994; 372: 770-3.
28. Critchley HD. Neural mechanisms of autonomic, affective, and cognitive integration. J Comp Neurol 2005; 493: 154-66.
29. Critchley HD, Mathias CJ, Josephs O, O'Doherty J, Zanini S, Dewar BK, et al. Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 2003; 126: 2139-52.
30. Dalmose AL, Bjarkam CR, Sorensen JC, Djurhuus JC, Jorgensen TM. Effects of high frequency deep brain stimulation on urine storage and voiding function in conscious minipigs. Neurourol Urodyn 2004; 23: 265-72.
31. Dasgupta R, Critchley HD, Dolan RJ, Fowler CJ. Changes in brain activity following sacral neuromodulation for urinary retention. J Urol 2005; 174: 2268-72.
32. de Groat WC, Nadelhaft I, Milne RJ, Booth AM, Morgan C, Thor K. Organization of the sacral parasympathetic reflex pathways to the urinary bladder and large intestine. J Auton Nerv Syst 1981; 3: 135-60.
33. Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schafer H, Botzel K, et al. A randomized trial of deep-brain stimulation for Parkinson's disease. N Engl J Med 2006; 355: 896-908.
34. Eickhoff SB, Lotze M, Wietek B, Amunts K, Enck P, Zilles K. Segregation of visceral and somatosensory afferents: an fMRI and cytoarchitectonic mapping study. Neuroimage 2006; 31: 1004-14.
35. Evans A, Kamber M, Collins D, MacDonald D. An MRI-based probalistic atlas of neuroanatomy. In: Shorvton S, Fish D, Andersmann F, Bydder G, Stefan H, editors. Magnetic resonance scanning and epilepsy. New York: Plenum Press; 1994. p. 263-74.
36. Finazzi-Agro E, Peppe A, D'Amico A, Petta F, Mazzone P, Stanzione P, et al. Effects of subthalamic nucleus stimulation on urodynamic findings in patients with Parkinson's disease. J Urol 2003; 169: 1388-91.
37. Friston K, Ashburner J, Frith C, Poline J, Heather K, Frackowiak R. Spatial registration and normalization of images. Hum Brain Mapp 1995a; 3: 165-89.
38. Friston K, Holmes A, Worsley K, Poline J, Frith C, Frackowiak R. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 1995b; 2: 189-210.
39. Friston KJ. Testing for anatomically specified regional effects. Hum Brain Mapp 1997; 5: 133-6.
40. Griffiths DJ. Cerebral control of bladder function. Curr Urol Rep 2004; 5: 348-52.
41. Hattori T, Yasuda K, Kita K, Hirayama K. Voiding dysfunction in Parkinson's disease. Jpn J Psychiatry Neurol 1992; 46: 181-6.
42. Herrero MT, Insausti R, Gonzalo LM. Cortically projecting cells in the periaqueductal gray matter of the rat. A retrograde fluorescent tracer study. Brain Res 1991; 543: 201-12.
43. Herzog J, Weiss PH, Assmus A, Wefer B, Seif C, Braun PM, et al. Subthalamic stimulation modulates cortical control of urinary bladder in Parkinson's disease. Brain 2006; 129: 3366-75.
44. Holstege G, Mouton LJ. Central nervous system control of micturition. Int Rev Neurobiol 2003; 56: 123-45.
45. Horn AC, Vahle-Hinz C, Bruggemann J, Petersen M, Kniffki KD. Responses of neurons in the lateral thalamus of the cat to stimulation of urinary bladder, colon, esophagus, and skin. Brain Res 1999; 851: 164-74.
46. Jobst EE, Melnick ME, Byl NN, Dowling GA, Aminoff MJ. Sensory perception in Parkinson disease. Arch Neurol 1997; 54: 450-4.
47. Kaji R, Urushihara R, Murase N, Shimazu H, Goto S. Abnormal sensory gating in basal ganglia disorders. J Neurol 2005; 252 (Suppl 4): IV13-6.
48. Kavia RB, Dasgupta R, Fowler CJ. Functional imaging and the central control of the bladder. J Comp Neurol 2005; 493: 27-32.
49. Koller WC. Sensory symptoms in Parkinson's disease. Neurology 1984; 34: 957-9.
50. Konczak J, Krawczewski K, Tuite P, Maschke M. The perception of passive motion in Parkinson's disease. J Neurol 2007; 254: 655-63.
51. Krout KE, Loewy AD. Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 2000; 424: 111-41.
52. Kuhtz-Buschbeck JP, van der Horst C, Pott C, Wolff S, Nabavi A, Jansen O, et al. Cortical representation of the urge to void: a functional magnetic resonance imaging study. J Urol 2005; 174: 1477-81.
53. Ladabaum U, Minoshima S, Hasler WL, Cross D, Chey WD, Owyang C. Gastric distention correlates with activation of multiple cortical and subcortical regions. Gastroenterology 2001; 120: 369-76.
54. Le Masson G, Renaud-Le Masson S, Debay D, Bal T. Feedback inhibition controls spike transfer in hybrid thalamic circuits. Nature 2002; 417: 854-8.
55. Lemack GE, Dewey RB Jr, Roehrborn CG, O'Suilleabhain PE, Zimmern PE. Questionnaire-based assessment of bladder dysfunction in patients with mild to moderate Parkinson's disease. Urology 2000; 56: 250-4.
56. Limousin P, Greene J, Pollak P, Rothwell J, Benabid AL, Frackowiak R. Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson's disease. Ann Neurol 1997; 42: 283-91.
57. Liu Z, Sakakibara R, Nakazawa K, Uchiyama T, Yamamoto T, Ito T, et al. Micturition-related neuronal firing in the periaqueductal gray area in cats. Neuroscience 2004; 126: 1075-82.
58. Mallory B, Steers WD, De Groat WC. Electrophysiological study of micturition reflexes in rats. Am J Physiol 1989; 257: R410-21.
59. Maschke M, Gomez CM, Tuite PJ, Konczak J. Dysfunction of the basal ganglia, but not the cerebellum, impairs kinaesthesia. Brain 2003; 126: 2312-22.
60. Maschke M, Tuite PJ, Pickett K, Wachter T, Konczak J. The effect of subthalamic nucleus stimulation on kinaesthesia in Parkinson's disease. J Neurol Neurosurg Psychiatry 2005; 76: 569-71.
61. Matsuura S, Kakizaki H, Mitsui T, Shiga T, Tamaki N, Koyanagi T. Human brain region response to distention or cold stimulation of the bladder: a positron emission tomography study. J Urol 2002; 168: 2035-9.
62. Meller ST, Dennis BJ. Afferent projections to the periaqueductal gray in the rabbit. Neuroscience 1986; 19: 927-64.
63. Morgan C, Nadelhaft I, de Groat WC. The distribution of visceral primary afferents from the pelvic nerve to Lissauer's tract and the spinal gray matter and its relationship to the sacral parasympathetic nucleus. J Comp Neurol 1981; 201: 415-40.
64. Mouton LJ, Holstege G. Segmental and laminar organization of the spinal neurons projecting to the periaqueductal gray (PAG) in the cat suggests the existence of at least five separate clusters of spino-PAG neurons. J Comp Neurol 2000; 428: 389-410.
65. Muller T, Woitalla D, Peters S, Kohla K, Przuntek H. Progress of visual dysfunction in Parkinson's disease. Acta Neurol Scand 2002; 105: 256-60.
66. Murnaghan GF, Millard RJ. Urodynamic evaluation of bladder neck obstruction in chronic prostatitis. Br J Urol 1984; 56: 713-6.
67. Nishizawa O, Ebina K, Sugaya K, Noto H, Satoh K, Kohama T, et al. Effect of cerebellectomy on reflex micturition in the decerebrate dog as determined by urodynamic evaluation. Urol Int 1989; 44: 152-6.
68. Noto H, Roppolo JR, Steers WD, de Groat WC. Electrophysiological analysis of the ascending and descending components of the micturition reflex pathway in the rat. Brain Res 1991; 549: 95-105.
69. Nour S, Svarer C, Kristensen JK, Paulson OB, Law I. Cerebral activation during micturition in normal men. Brain 2000; 123 (Pt 4): 781-9.
70. Onofrj M, Thomas A. Acute akinesia in Parkinson disease. Neurology 2005; 64: 1162-9.
71. O'Suilleabhain P, Bullard J, Dewey RB. Proprioception in Parkinson's disease is acutely depressed by dopaminergic medications. J Neurol Neurosurg Psychiatry 2001; 71: 607-10.
72. Pekkonen E, Ahveninen J, Virtanen J, Teravainen H. Parkinson's disease selectively impairs preattentive auditory processing: an MEG study. Neuroreport 1998; 9: 2949-52.
73. Philipova D, Gatchev G, Vladova T, Georgiev D. Event-related potentials in parkinsonian patients under auditory discrimination tasks. Int J Psychophysiol 1997; 27: 69-78.
74. Pinault D. The thalamic reticular nucleus: structure, function and concept. Brain Res Brain Res Rev 2004; 46: 1-31.
75. Pleger B, Dinse HR, Ragert P, Schwenkreis P, Malin JP, Tegenthoff M. Shifts in cortical representations predict human discrimination improvement. Proc Natl Acad Sci USA 2001; 98: 12255-60.
76. Porter RW, Bors E. Neurogenic bladder in parkinsonism: effect of thalamotomy. J Neurosurg 1971; 34: 27-32.
77. Potter M, Illert M, Wenzelburger R, Deuschl G, Volkmann J. The effect of subthalamic nucleus stimulation on autogenic inhibition in Parkinson disease. Neurology 2004; 63: 1234-9.
78. Sailer A, Cunic DI, Paradiso GO, Gunraj CA, Wagle-Shukla A, Moro E, et al. Subthalamic nucleus stimulation modulates afferent inhibition in Parkinson disease. Neurology 2007; 68: 356-63.
79. Sakakibara R, Hattori T, Uchiyama T, Yamanishi T. Videourodynamic and sphincter motor unit potential analyses in Parkinson's disease and multiple system atrophy. J Neurol Neurosurg Psychiatry 2001; 71: 600-6.
80. Sathian K, Zangaladze A, Green J, Vitek JL, DeLong MR. Tactile spatial acuity and roughness discrimination: impairments due to aging and Parkinson's disease. Neurology 1997; 49: 168-77.
81. Schneider E, Patras L, Fischer PA. Neurogenic bladder disturbances in Parkinson's disease (author's transl). Fortschr Neurol Psychiatr Grenzgeb 1978; 46: 260-8.
82. Schneider JS, Diamond SG, Markham CH. Deficits in orofacial sensorimotor function in Parkinson's disease. Ann Neurol 1986; 19: 275-82.
83. Schneider JS, Diamond SG, Markham CH. Parkinson's disease: sensory and motor problems in arms and hands. Neurology 1987; 37: 951-6.
84. Schrader B, Hamel W, Weinert D, Mehdorn HM. Documentation of electrode localization. Mov Disord 2002; 17 (Suppl 3): S167-74.
85. Schwarz M, Block F, Topper R, Sontag KH, Noth J. Abnormalities of somatosensory evoked potentials in the quinolinic acid model of Huntington's disease: evidence that basal ganglia modulate sensory cortical input. Ann Neurol 1992; 32: 358-64.
86. Seif C, Herzog J, van der Horst C, Schrader B, Volkmann J, Deuschl G, et al. Effect of subthalamic deep brain stimulation on the function of the urinary bladder. Ann Neurol 2004; 55: 118-20.
87. Shammah-Lagnado SJ, Alheid GF, Heimer L. Efferent connections of the caudal part of the globus pallidus in the rat. J Comp Neurol 1996; 376: 489-507.
88. Shelley BP, Trimble MR. The insular lobe of Reil - its anatamico-functional, behavioural and neuropsychiatric attributes in humans - a review. World J Biol Psychiatry 2004; 5: 176-200.
89. Shin HW, Kang SY, Sohn YH. Dopaminergic influence on disturbed spatial discrimination in Parkinson's disease. Mov Disord 2005; 20: 1640-3.
90. Shivitz N, Koop MM, Fahimi J, Heit G, Bronte-Stewart HM. Bilateral subthalamic nucleus deep brain stimulation improves certain aspects of postural control in Parkinson's disease, whereas medication does not. Mov Disord 2006; 21: 1088-97.
91. Shulman LM, Taback RL, Bean J, Weiner WJ. Comorbidity of the nonmotor symptoms of Parkinson's disease. Mov Disord 2001; 16: 507-10.
92. Snider SR, Fahn S, Isgreen WP, Cote LJ. Primary sensory symptoms in parkinsonism. Neurology 1976; 26: 423-9.
93. Strafella AP, Dagher A, Sadikot AF. Cerebral blood flow changes induced by subthalamic stimulation in Parkinson's disease. Neurology 2003; 60: 1039-42.
94. Thobois S, Dominey P, Fraix V, Mertens P, Guenot M, Zimmer L, et al. Effects of subthalamic nucleus stimulation on actual and imagined movement in Parkinson's disease: a PET study. J Neurol 2002; 249: 1689-98.
95. Thomas A, Iacono D, Luciano AL, Armellino K, Onofrj M. Acute akinesia or akinetic crisis in Parkinson's disease. Neurol Sci 2003; 24: 219-20.
96. Vanderhorst VG, Mouton LJ, Blok BF, Holstege G. Distinct cell groups in the lumbosacral cord of the cat project to different areas in the periaqueductal gray. J Comp Neurol 1996; 376: 361-85.
97. Weiss PH, Marshall JC, Zilles K, Fink GR. Are action and perception in near and far space additive or interactive factors? Neuroimage 2003; 18: 837-46.
98. Winge K, Fowler CJ. Bladder dysfunction in Parkinsonism: mechanisms, prevalence, symptoms, and management. Mov Disord 2006; 21: 737-45.
99. Witjas T, Kaphan E, Regis J, Jouve E, Cherif AA, Peragut JC, et al. Effects of chronic subthalamic stimulation on nonmotor fluctuations in Parkinson's disease. Mov Disord 2007; 22: 1729-34.
100. Worsley K, Marret S, Neelin P, vandal A, Friston K, Evans A. A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 1996; 4: 58-73.
101. Yingling CD, Skinner JE. Selective regulation of thalamic sensory relay nuclei by nucleus reticularis thalami. Electroencephalogr Clin Neurophysiol 1976; 41: 476-82.
102. Zia S, Cody F, O'Boyle D. Joint position sense is impaired by Parkinson's disease. Ann Neurol 2000; 47: 218-28.