Functional evaluation of central cholinergic circuits in patients with Parkinson's disease and REM sleep behavior disorder: A TMS study

Journal of Neural Transmission

Volumn 120, Issue 3, 2013, Pages 413-422

  Nardone, Raffaele ^a,b   Bergmann, Jürgen ^c   Brigo, Francesco ^b,d   Christova, Monica ^e   Kunz, Alexander ^a   Seidl, Martin ^a   Tezzon, Frediano ^b   Trinka, Eugen ^a   Golaszewski, Stefan ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b Department of Laboratory and Internal Medicine   (Italy)

^c Christian Doppler Klinik   (Austria)

^d UNIVERSITY OF VERONA   (Italy)

^e MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

Parkinson's disease; REM sleep behavior disorder; Short latency afferent inhibition; Transcranial magnetic stimulation

Indexed keywords

LEVODOPA;

ADULT; AGED; ARTICLE; CHOLINERGIC SYSTEM; CLINICAL ARTICLE; CONDITIONING; CONTROLLED STUDY; DISEASE DURATION; EPISODIC MEMORY; EVOKED SOMATOSENSORY RESPONSE; EXCITABILITY; EXECUTIVE FUNCTION; FEMALE; HUMAN; LATENT PERIOD; MALE; MEDIAN NERVE; MILD COGNITIVE IMPAIRMENT; MINI MENTAL STATE EXAMINATION; MOTOR CORTEX; MUSCLE RELAXATION; NEUROPSYCHOLOGICAL TEST; PARASOMNIA; PARKINSON DISEASE; PRIORITY JOURNAL; REM SLEEP; TRANSCRANIAL MAGNETIC STIMULATION; VERBAL MEMORY;

AGED; BRAIN; CHOLINERGIC FIBERS; FEMALE; HUMANS; MALE; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; PARKINSON DISEASE; REM SLEEP BEHAVIOR DISORDER; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84875754605     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-012-0888-6     Document Type: Article

References (74)

1. American Academy of Sleep Medixine, Task Forse Chair; Hauri PJ, Chairman (2005) The international classification of sleep disorders: diagnostic and coding manual, 2nd edn. American Academy of Sleep Medicine, Westchester
2. Arnulf I, Bonnet AM, Damier P, Bejjani BP, Seilhean D, Derenne JP, Agid Y (2000) Hallucinations, REM sleep, and Parkinson's disease: a medical hypothesis. Neurology 55:281-288 (Pubitemid 30604632)
3. Aston-Jones G, Rajkowski J, Cohen J (1999) Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry 46:1309-1320 (Pubitemid 30114448)
4. Babiloni C, Binetti G, Cassetta E, Dal Forno G, Del Percio C, Ferreri F, Ferri R, Frisoni G, Hirata K, Lanuzza B, Miniussi C, Moretti DV, Nobili F, Rodriguez G, Romani GL, Salinari S, Rossini PM (2006) Sources of cortical rhythms change as a function of cognitive impairment in pathological aging: a multicenter study. Clin Neurophysiol 117:252-268 (Pubitemid 43228015)
5. Beck AT, Steer RA, Brown GK (1996) The Beck depression inventory, 2nd edn. The Psychological Corporation, San Antonio
6. Berridge CW, Page ME, Valentino RJ, Foote SL (1993) Effects of locus coeruleus inactivation on electroencephalographic activity in neocortex and hippocampus. Neuroscience 55:381-393 (Pubitemid 23211350)
7. Boeve BF, Silber MH, Ferman TJ, Lucas JA, Parisi JE (2001) Association of REM sleep behavior disorder and neurodegenerative disease may reflect an underlying synucleinopathy. Mov Disord 16:622-630 (Pubitemid 36040841)
8. Bohnen NI, Kaufer DI, Hendrickson R, Ivanco LS, Lopresti BJ, Constantine GM, Mathis ChA, Davis JG, Moore RY, Dekosky ST (2006) Cognitive correlates of cortical cholinergic denervation in Parkinson's disease and Parkinsonian dementia. J Neurol 253:242-247 (Pubitemid 43255898)
9. Braak H, Rüb U, Jansen Steur EN, Del Tredici K, de Vos RA (2005) Cognitive status correlates with neuropathologic stage in Parkinson disease. Neurology 64:1404-1410 (Pubitemid 40570509)
10. Comella CL, Nardine TM, Diederich NJ, Stebbins GT (1998) Sleep-related violence, injury, and REM sleep behavior disorder in Parkinson's disease. Neurology 51:526-529 (Pubitemid 28406332)
11. Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Di Giovanni S, Zito G, Tonali P, Rothwell JC (2000) Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex. Exp Brain Res 135:455-461
12. Di Lazzaro V, Oliviero A, Tonali PA, Marra C, Daniele A, Profice P, Saturno E, Pilato F, Masullo C, Rothwell JC (2002) Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation. Neurology 59:392-397 (Pubitemid 34857932)
13. Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Pilato F, Zito G, Dileone M, Nicoletti R, Pasqualetti P, Tonali PA (2003) Ketamine increases human motor cortex excitability to transcranial magnetic stimulation. J Physiol 547:485-496 (Pubitemid 36304982)
14. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Bentivoglio AR, Tonali A (2004a) Normal or enhanced short-latency afferent inhibition in Parkinson's disease? Brain 127:E8
15. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Marra C, Daniele A, Ghirlanda S, Gainotti G, Tonali PA (2004b) Motor cortex excitability to transcranial magnetic stimulation in Alzheimer's disease. J Neurol Neurosurg Psychiatry 75:555-559 (Pubitemid 38406651)
16. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Marra C, Ghirlanda S, Ranieri F, Gainotti G, Tonali (2005a) Neurophysiological predictors of long term response to AChE inhibitors in AD patients. J Neurol Neurosurg Psychiatry 76:1064-1069 (Pubitemid 41081276)
17. Di Lazzaro V, Oliviero A, Saturno E, Di leone M, Pilato F, Nardone R, Ranieri F, Musumeci G, Fiorilla T, Tonali P (2005b) Effects of lorazepam on short latency afferent inhibition and short latency intracortical inhibition in humans. J Physiol 564:661-668 (Pubitemid 40585061)
18. Di Lazzaro V, Pilato F, Dileone M, Tonali PA, Ziemann U (2005c) Dissociated effects of diazepam and lorazepam on short-latency afferent inhibition. J Physiol 569:315-323 (Pubitemid 41701394)
19. Di Lazzaro V, Pilato F, Dileone M, Saturno E, Oliviero A, Marra C, Daniele A, Ranieri F, Gainotti G, Tonali PA (2006) In vivo cholinergic circuit evaluation in frontotemporal and Alzheimer dementias. Neurology 66:1111-1113 (Pubitemid 44044806)
20. Di Lazzaro V, Pilato F, Dileone M, Saturno E, Profice P, Marra C, Daniele A, Ranieri F, Quaranta D, Gainotti G, Tonali PA (2007) Functional evaluation of cerebral cortex in dementia with Lewy bodies. Neuroimage 37(2):422-429 (Pubitemid 47444261)
21. Emre M (2003) Dementia associated with Parkinson's disease. Lancet Neurol 2:229-237 (Pubitemid 37443310)
22. Fahn S, Elton RL, members of the UPDRS Development Committee. Unified Parkinson's Disease Rating Scale (1987) In: Fahn S, Marsden CD, Calne DB, Liebermann A (eds) Recent developments in Parkinson's disease. Macmillan Health Care Information, Florham Park, pp 153-163
23. Fantini ML, Gagnon JF, Petit D, Rompré S, Décary A, Carrier J, Montplaisir J (2003) Slowing of electroencephalogram in rapid eye movement sleep behavior disorder. Ann Neurol 53(6):774-780 (Pubitemid 36622515)
24. Ferini-Strambi L, Di Gioia MR, Castronovo V, Oldani A, Zucconi M, Cappa SF (2004) Neuropsychological assessment in idiopathic REM sleep behavior disorder (RBD): does the idiopathic form of RBD really exist? Neurology 62(1):41-45 (Pubitemid 38082868)
25. Foltynie T, Brayne CE, Robbins TW, Barker RA (2004) The cognitive ability of an incident cohort of Parkinson's patients in the UK. The CamPaIGN study. Brain 127:550-560 (Pubitemid 38295472)
26. Fujiki M, Hikawa T, Abe T, Ishii K, Kobayashi H (2006) Reduced short latency afferent inhibition in diffuse axonal injury patients with memory impairment. Neurosci Lett 405:226-230 (Pubitemid 44189721)
27. Gagnon JF, Bedard MA, Fantini ML, Petit D, Panisset M, Rompré S, Carrier J, Montplaisir J (2002a) REM sleep behavior disorder and REM sleep without atonia in Parkinson's disease. Neurology 59:585-589 (Pubitemid 34919994)
28. Gagnon JF, Montplaisir J, Bédard MA (2002b) Les troubles du sommeil paradoxal dans la maladie de Parkinson. Rev Neurol 158:135-152 (Pubitemid 34204567)
29. Gagnon JF, Fantini ML, Bedard MA, Petit D, Carrier J, Rompré S, Décary A, Panisset M, Montplaisir J (2004) Association between waking EEG slowing and REM sleep behavior disorder in PD without dementia. Neurology 62:401-406 (Pubitemid 38200850)
30. Glenville M, Wilkinson RT (1979) Portable devices for measuring performance in the field: the effects of sleep deprivation and might shift on the performance of computer operators. Ergonomics 22:927-933 (Pubitemid 10188590)
31. Green J, McDonald WM, Vitek JL, Evatt M, Freeman A, Haber M, Bakay RA, Triche S, Sirockman B, DeLong MR (2002) Cognitive impairments in advanced PD without dementia. Neurology 59:1320-1324 (Pubitemid 35285980)
32. Helkala EL, Laulumaa V, Soininen H, Riekkinen PJ (1988) Recall and recognition memory in patients with Alzheimer's and Parkinson's diseases. Ann Neurol 24:214-217
33. Hendricks JC, Morrison AR, Mann GL (1982) Different behaviors during paradoxical sleep without atonia depend on pontine lesion site. Brain Res 239:81-105 (Pubitemid 12101770)
34. Hilker R, Thomas AV, Klein JC, Weisenbach S, Kalbe E, Burghaus L, Jacobs AH, Herholz K, Heiss WD (2005) Dementia in Parkinson disease: functional imaging of cholinergic and dopaminergic pathways. Neurology 65:1716-1722
35. Inglis WL, Olmstead MC, Robbins TW (2001) Selective deficits in attentional performance on the 5-choice serial reaction time task following pedunculopontine tegmental nucleus lesions. Behav Brain Res 123:117-131 (Pubitemid 32496511)
36. Iranzo A, Molinuevo JL, Santamaria J, Serradell M, Martí MJ, Valldeoriola F, Tolosa E (2006) Rapid-eye-movement sleep behaviour disorder as an early marker for a neurodegenerative disorder: a descriptive study. Lancet Neurol 5:572-577 (Pubitemid 43867426)
37. Janvin C, Aarsland D, Larsen JP, Hugdahl K (2003) Neuropsychological profile of patients with Parkinson's disease without dementia. Dement Geriatr Cogn Disord 15:126-131 (Pubitemid 36206641)
38. Janvin CC, Larsen JP, Aarsland D, Hugdahl K (2006) Subtypes of mild cognitive impairment in Parkinson's disease. Mov Disord 21(9):1343-1349 (Pubitemid 44613283)
39. Jones BE (2000) Basic mechanisms of sleep-wake states. In: Kryger MH, Roth T, Dement WC (eds) Principles and practice of sleep medicine, 3rd edn. Saunders, Philadelphia, pp 134-154
40. Jouvet M, Delorme F (1965) Locus coeruleus et sommeil paradoxal. C R Soc Biol 159:895-899
41. Kleiner S, Bringmann A (1996) Nucleus basalis magnocellularis and pedunculopontine tegmental nucleus: control of the slow EEG waves in rats. Arch Ital Biol 134:153-167 (Pubitemid 26129104)
42. Kimura J, Daube J, Burke D, Hallett M, Cruccu G, Ongerboer de Visser BW, Yanagisawa N, Shimamura M, Rothwell J (1994) Human reflexes and late responses. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 40:393-403 (Pubitemid 24201255)
43. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501-519 (Pubitemid 23345592)
44. Levin BE, Llabre MM, Reisman S, Weiner WJ, Sanchez-Ramos J, Singer C, Brown MC (1991) Visuospatial impairment in Parkinson's disease. Neurology 41:365-369
45. Lezak MD, Howieson DB, Loring DW (2004) Neuropsychological assessment, 4th edn. Oxford University Press, New York
46. Mahowald MW, Schenck CH (2000) REM sleep parasomnias. In: Kryger MH, Roth T, Dement WC (eds) Principles and practice of sleep medicine, 3rd edn. Saunders, Philadelphia, pp 724-741
47. Manganelli F, Vitale C, Santangelo G, Pisciotta C, Iodice R, Cozzolino A, Dubbioso R, Picillo M, Barone P, Santoro L (2009) Functional involvement of central cholinergic circuits and visual hallucinations in Parkinson's disease. Brain 132(Pt 9):2350-2355
48. Martorana A, Mori F, Esposito Z, Kusayanagi H, Monteleone F, Codecà C, Sancesario G, Bernardi G, Koch G (2009) Dopamine modulates cholinergic cortical excitability in Alzheimer's disease patients. Neuropsychopharmacology 34(10):1328-2323
49. Massicotte-Marquez J, Décary A, Gagnon JF, Vendette M, Mathieu A, Postuma RB, Carrier J, Montplaisir J (2008) Executive dysfunction and memory impairment in idiopathic REM sleep behavior disorder. Neurology 70(15):1250-1257 (Pubitemid 351520966)
50. Muslimovic D, Post B, Speelman JD, Schmand B (2005) Cognitive profile of patients with newly diagnosed Parkinson disease. Neurology 65:1239-1245 (Pubitemid 41508217)
51. Nardone R, Florio I, Lochner P, Tezzon F (2005) Cholinergic cortical circuits in Parkinson's disease and in progressive supranuclear palsy: a transcranial magnetic stimulation study. Exp Brain Res 163:128-131 (Pubitemid 40868524)
52. Nardone R, Bergmann J, Christova M, Caleri F, Tezzon F, Ladurner G, Trinka E, Golaszewski S (2012a) Short latency afferent inhibition differs among the subtypes of mild cognitive impairment. J Neural Transm 119(4):463-471
53. Nardone R, Bergmann J, Kunz A, Christova M, Brigo F, Tezzon F, Trinka E, Golaszewski S (2012b) Cortical afferent inhibition is reduced in patients with idiopathic REM sleep behavior disorder and cognitive impairment. Sleep Med 13(7):919-925
54. Perry E, Walker M, Grace J, Perry R (1999) Acetylcholine in mind: a neurotransmitter correlate of consciousness? Trends Neurosci 22:273-280 (Pubitemid 29259995)
55. Postuma RB, Gagnon JF, Vendette M, Montplaisir JY (2009) Idiopathic REM sleep behavior disorder in the transition to denerative disease. Mov Disord 24(15):2225-2232
56. Postuma RB, Bertrand JA, Montplaisir J, Desjardins C, Vendette M, Rios Romenets S, Panisset M, Gagnon JF (2012) Rapid eye movement sleep behavior disorder and risk of dementia in Parkinson's diesease: a prospective study. Mov Disord 27(6):720-726
57. Petersen RC, Morris JC (2005) Mild cognitive impairment as a clinical entity and treatment target. Arch Neurol 62(7):1160-1163 (Pubitemid 41043744)
58. Prichep LS, John ER, Ferris SH, Reisberg B, Almas M, Alper K, Cancro R (1994) Quantitative EEG correlates of cognitive deterioration in the elderly. Neurobiol Aging 15:85-90 (Pubitemid 24075015)
59. Rossini PM, Barker T, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic MR, Hallett M, Katayama Y, Lucking CH, Maertens de Noordhout AL, Marsden CD, Murray NMF, Rothwell JC, Swash M, Tomberg C (1994) Non invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application: report of IFCN committee. Electroenceph Clin Neurophysiol 91:79-92 (Pubitemid 24246462)
60. Rowe JB, Hughes L, Ghosh BC, Eckstein D, Williams-Gray CH, Fallon S, Barker RA, Owen AM (2008) Parkinson's disease and dopaminergic therapy - differential effects on movement, reward and cognition. Brain 131(Pt 8):2094-2105
61. Sailer A, Molnar GF, Paradiso G, Gunraj CA, Lang AE, Chen R (2003) Short and long latency afferent inhibition in Parkinson's disease. Brain 26:1883-1894 (Pubitemid 36917347)
62. Schenck CH, Bundlie SR, Mahowald MW (1996a) Delayed emergence of a parkinsonian disorder in 38% of 29 older men initially diagnosed with idiopathic rapid eye movement sleep behavior disorder. Neurology 46:388-393
63. Schenck CH, Garcia-Rill E, Skinner RD, Anderson ML, Mahowald MW (1996b) A case of REM sleep behavior disorder with autopsy-confirmed Alzheimer's disease: post-mortem brain stem histochemical analyses. Biol Psychiatry 40:422-425 (Pubitemid 26301076)
64. Steckler T, Inglis W, Winn P, Sahgal A (1994) The pedunculopontine tegmental nucleus: a role in cognitive processes? Brain Res Rev 19:298-318 (Pubitemid 24262982)
65. Terzaghi M, Sinforiani E, Zucchella C, Zambrelli E, Pasotti C, Rustioni V, Manni R (2008) Cognitive performance in REM sleep behaviour disorder: a possible early marker of neurodegenerative disease? Sleep Med 9(4):343-351 (Pubitemid 351664082)
66. Tokimura H, Di Lazzaro V, Tokimura Y, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (2000) Short latency inhibition of human hand motor cortex by somatosensory input from the hand. J Physiol 523:503-513 (Pubitemid 30137656)
67. Turner RS, D'Amato CJ, Chervin RD, Blaivas M (2000) The pathology of REM sleep behavior disorder with comorbid Lewy body dementia. Neurology 55:1730-1732
68. Uchiyama M, Isse K, Tanaka K, Yokota N, Hamamoto M, Aida S, Ito Y, Yoshimura M, Okawa M (1995) Incidental Lewy body disease in a patient with REM sleep behavior disorder. Neurology 45:709-712
69. Vendette M, Gagnon JF, Décary A, Massicotte-Marquez J, Postuma RB, Doyon J, Panisset M, Montplaisir J (2007) REM sleep behavior disorder predicts cognitive impairment in Parkinson disease without dementia. Neurology 69(19):1843-1849 (Pubitemid 350071145)
70. Wilkinson RT, Houghton D (1975) Portable four-choise reaction timewith magnetic tape memory. Behav Res Methods Instum 7:441-446
71. Williams-Gray CH, Hampshire A, Robbins TW, Owen AM, Barker RA (2007) Catechol O-methyltransferease Vall58Met genotyper influences frontoparietal activity during planning in patients with Parkinson's disease. J Neurosci 27(18):4832-4838 (Pubitemid 46699066)
72. Winn P (1998) Frontal syndrome as a consequence of lesions in the pedunculopontine tegmental nucleus: a short theoretical review. Brain Res Bull 47:551-563 (Pubitemid 29115368)
73. Ziemann U, Lonnecker S, Steinhoff BH, Paulus W (1996) Effects of antiepileptics drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:367-378 (Pubitemid 26304794)
74. Ziemann U, Paulus W, Nitsche MA, Pascual-Leone A, Byblow WD, Berardelli A, Siebner HR, Classen J, Cohen LG, Rothwell JC (2008) Consensus: motor cortex plasticity protocols. Brain Stimul 1:164-182