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Journal of Neural Transmission
Published in: Journal of Neural Transmission 11/2017

01-11-2017 | Neurology and Preclinical Neurological Studies - Review Article

Cortical afferent inhibition abnormalities reveal cholinergic dysfunction in Parkinson’s disease: a reappraisal

Authors: Raffaele Nardone, Francesco Brigo, Viviana Versace, Yvonne Höller, Frediano Tezzon, Leopold Saltuari, Eugen Trinka, Luca Sebastianelli

Published in: Journal of Neural Transmission | Issue 11/2017

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Abstract

Parkinson’s disease (PD) is a multisystem neurodegenerative disorder affecting, besides the dopaminergic function, multiple neurotransmission systems, including the cholinergic system. Central cholinergic circuits of human brain can be tested non-invasively by coupling peripheral nerve stimulation with transcranial magnetic stimulation (TMS) of motor cortex; this test is named short latency afferent inhibition (SAI). SAI abnormalities have been reported in PD patients with gait disturbances and many non-motor symptoms, such as visual hallucinations (VHs), REM sleep behavior disorder (RBD), dysphagia, and olfactory impairment. The findings of these TMS studies strongly suggest that cholinergic degeneration is an important contributor to a number of clinical features of PD. TMS and neuropsychological raise the possibility that the presence of RBD, VHs and olfactory dysfunction indicate increased risk of cognitive impairment in patients with PD. Longitudinal studies of the patients are required to verify whether SAI abnormalities can predict a future severe cognitive decline. TMS can provide simple measures that may represent suitable biomarkers of cholinergic neurotransmission in PD. SAI studies enable an early recognition of PD patients with cholinergic system degeneration, and this might allow future targeted cholinergic treatment approaches, in addition to dopaminergic therapy, to ameliorate non-motor and motor clinical symptoms in PD patients.
Literature
Aarsland D, Andersen K, Larsen JP, Perry R, Wentzel-Larsen T, Lolk A, Kragh-Sørensen P (2004) The rate of cognitive decline in Parkinson disease. Arch Neurol 61:1906–1911PubMedCrossRef
Alexander GE (2004) Biology of Parkinson’s disease: pathogenesis and pathophysiology of a multisystem neurodegenerative disorder. Dialogues Clin Neurosci 6:259–280PubMedPubMedCentral
Arendt T, Bigl V, Arendt A, Tennstedt A (1983) Loss of neurons in the nucleus basalis of Meynert in Alzheimer’s disease, paralysis agitans and Korsakoff’s disease. Acta Neuropathol 61:101–108PubMedCrossRef
Asmussen MJ, Jacobs MF, Lee KG, Zapallow CM, Nelson AJ (2013) Short-latency afferent inhibition modulation during finger movement. PLoS One 4:e60496CrossRef
Asmussen MJ, Zapallow CM, Jacobs MF, Lee KG, Tsang P, Nelson AJ (2014) Modulation of short-latency afferent inhibition depends on digit and task-relevance. PLoS One 9:e104807PubMedPubMedCentralCrossRef
Berger-Sweeney J, Stearns NA, Frick KM, Beard B, Baxter MG (2000) Cholinergic basal forebrain is critical for social transmission of food preferences. Hippocampus 10:729–738PubMedCrossRef
Berlanga ML, Simpson TK, Alcantara AA (2005) Dopamine D5 receptor localization on cholinergic neurons of the rat forebrain and diencephalon: a potential neuroanatomical substrate involved in mediating dopaminergic influences on acetylcholine release. J Comp Neurol 492:34–49PubMedCrossRef
Bohnen NI, Albin RL (2011) The cholinergic system and Parkinson disease. Behav Brain Res 221:564–573PubMedCrossRef
Bohnen NI, Kaufer DI, Ivanco LS, Lopresti B, Koeppe RA, Davis JG, Mathis CA, Moore RY, DeKosky ST (2003) Cortical cholinergic function is more severely affected in parkinsonian dementia than in Alzheimer disease: an in vivo positron emission tomographic study. Arch Neurol 60:1745–1748PubMedCrossRef
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 253:242–247PubMedCrossRef
Bohnen NI, Frey KA, Studenski S, Kotagal V, Koeppe RA, Scott PJ, Albin RL, Müller ML (2013) Gait speed in Parkinson disease correlates with cholinergic degeneration. Neurology 81:1611–1616PubMedPubMedCentralCrossRef
Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211PubMedCrossRef
Braak H, Rüb U, Jansen Steur EN, Del Tredici K, de Vos RA (2005) Cognitive status correlates with neuropathologic stage in Parkinson disease. Neurology 64:1404–1410PubMedCrossRef
Braak E, Sandmann-Keil D, Rüb U, Gai WP, de Vos RA, Steur EN, Arai K, Braak H (2011) Alpha-synuclein immunopositive Parkinson’s disease-related inclusion bodies in lower brain stem nuclei. Acta Neuropathol 101:195–201
Broks P, Preston Traub M, Poppleton P, Ward C, Stahl SM (1988) Modelling dementia: effects of scopolamine on memory and attention. Neuropsychologia 26:685–700PubMedCrossRef
Candy JM, Perry RH, Perry EK, Irving D, Blessed G, Fairbairn AF, Tomlinson BE (1983) Pathological changes in the nucleus of Meynert in Alzheimer’s and Parkinson’s diseases. J Neurol Sci 59:277–289PubMedCrossRef
Cantone M, Di Pino G, Capone F, Piombo M, Chiarello D, Cheeran B, Pennisi G, Di Lazzaro V (2014) The contribution of transcranial magnetic stimulation in the diagnosis and in the management of dementia. Clin Neurophysiol 125:1509–1532PubMedCrossRef
Celebi O, Temucin CM, Elibol B, Saka E (2012) Short latency afferent inhibition in Parkinson’s disease patients with dementia. Mov Disord 27:1052–1055PubMedCrossRef
Cereda E, Cilia R, Klersy C, Canesi M, Zecchinelli AL, Mariani CB, Tesei S, Sacilotto G, Meucci N, Zini M, Isaias IU, Cassani E, Goldwurm S, Barichella M, Pezzoli G (2014) Swallowing disturbances in Parkinson’s disease: a multivariate analysis of contributing factors. Park Relat Disord 20:1382–1387CrossRef
Chung KA, Lobb BM, Nutt JG, Horak FB (2010) Effects of a central cholinesterase inhibitor on reducing falls in Parkinson disease. Neurology 75:1263–1269PubMedPubMedCentralCrossRef
Collerton D, Perry E, McKeith I (2005) Why people see things that are not there: a novel perception and attention deficit model for recurrent complex visual hallucinations. Behav Brain Sci 28:737–757PubMed
Compta Y, Parkkinen L, O’Sullivan SS, Vandrovcova J, Holton JL, Collins C, Lashley T, Kallis C, Williams DR, de Silva R, Lees AJ, Revesz T (2011) Lewy- and Alzheimer-type pathologies in Parkinson’s disease dementia: which is more important? Brain 134:1493–1505PubMedPubMedCentralCrossRef
Cromarty RA, Elder GJ, Graziadio S, Baker M, Bonanni L, Onofrj M, O’Brien JT, Taylor JP (2016) Neurophysiological biomarkers for Lewy body dementias. Clin Neurophysiol 127:349–359PubMedPubMedCentralCrossRef
De Rosa E, Hasselmo ME, Baxter MG (2000) Contribution of the cholinergic basal forebrain to proactive interference from stored odor memories during associative learning in rats. Behav Neurosci 115:314–327CrossRef
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 135:455–461PubMedCrossRef
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 59:392–397PubMedCrossRef
Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Bentivoglio AR, Tonali A (2004) Normal or enhanced short-latency afferent inhibition in Parkinsonʼs disease? Brain 127:E8PubMedCrossRef
Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Marra C, Ghirlanda S, Ranieri F, Gainotti G, Tonali P (2005) Neurophysiological predictors of long term response to AChE inhibitors in AD patients. J Neurol Neurosurg Psychiatry 76:1064–1069PubMedCrossRef
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 37:422–429PubMedCrossRef
Doty RL, Bagla R, Kim N (1999) Physostigmine enhances performance on an odor mixture discrimination test. Physiol Behav 65:801–804PubMedCrossRef
Dugger BN, Murray ME, Boeve BF, Parisi JE, Benarroch EE, Ferman TJ, Dickson DW (2012) Neuropathological analysis of brainstem cholinergic and catecholaminergic nuclei in relation to rapid eye movement (REM) sleep behaviour disorder. Neuropathol Appl Neurobiol 38:142–152PubMedPubMedCentralCrossRef
Fénelon G, Mahieux F, Huon R, Ziégler M (2000) Hallucinations in Parkinson’s disease: prevalence, phenomenology and risk factors. Brain 123:733–745PubMedCrossRef
Fletcher ML, Wilson DA (2002) Experience modifies olfactory acuity: acetylcholine-dependent learning decreases behavioral generalization between similar odorants. J Neurosci 22:1–5
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 405:226–230PubMedCrossRef
Fullard ME, Tran B, Xie SX, Toledo JB, Scordia C, Linder C, Purri R, Weintraub D, Duda JE, Chahine LM, Morley JF (2016) Olfactory impairment predicts cognitive decline in early Parkinson’s disease. Park Relat Disord 25:45–51CrossRef
Furey ML, Pietrini P, Haxby JV, Drevets WC (2008) Selective effects of cholinergic modulation on task performance during selective attention. Neuropsychopharmacology 33:913–923PubMedCrossRef
Gaspar P, Gray F (1984) Dementia in idiopathic Parkinson’s disease. A neuropathology I study of 32 cases. Acta Neuropathol (Bed) 64:43–52CrossRef
Goetz CG, Ouyang B, Negron A, Stebbins GT (2010) Hallucinations and sleep disorders in PD: ten-year prospective longitudinal study. Neurology 75:1773–1779PubMedPubMedCentralCrossRef
Grossi D, Trojano L, Pellecchia MT, Amboni M, Fragassi NA, Barone P (2005) Frontal dysfunction contributes to the genesis of hallucinations in non-demented Parkinsonian patients. Int J Geriatr Psychiatry 20:668–673PubMedCrossRef
Haehner A, Boesveldt S, Berendse HW, Mackay-Sim A, Fleischmann J, Silburn PA, Johnston AN, Mellick GD, Herting B, Reichmann H, Hummel T (2009) Prevalence of smell loss in Parkinson’s disease—a multicenter study. Park Relat Disord 15:490–494CrossRef
Halliday GM, Li YW, Blumbergs PC, Joh TH, Cotton RG, Howe PR, Blessing WW, Geffen LB (1990) Neuropathology of immunohistochemically identified brainstem neurons in Parkinson’s disease. Ann Neurol 27:373–385PubMedCrossRef
Han L, McCusker J, Cole M, Abrahamowicz M, Primeau F, Elie M (2001) Use of medications with anticholinergic effect predicts clinical severity of delirium symptoms in older medical inpatients. Arch Intern Med 161:1099–1105PubMedCrossRef
Hepp DH, Ruiter AM, Galis Y, Voorn P, Rozemuller AJ, Berendse HW, Foncke EM, van de Berg WD (2013) Pedunculopontine cholinergic cell loss in hallucinating Parkinson disease patients but not in dementia with Lewy bodies patients. J Neuropathol Exp Neurol 72:1162–1170PubMedCrossRef
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 265:1716–1722CrossRef
Hobson P, Meara J (2004) Risk and incidence of dementia in a cohort of older subjects with Parkinson’s disease in the United Kingdom. Mov Disord 19:1043–1049PubMedCrossRef
Hunter AJ, Murray TK (1989) Cholinergic mechanisms in a simple test of olfactory learning in the rat. Psychopharmacology 81:270–275CrossRef
Hunter PC, Crameri J, Austin S, Woodward MC, Hughes AJ (1997) Response of parkinsonian swallowing dysfunction to dopaminergic stimulation. J Neurol Neurosurg Psychiatry 63:579–583PubMedPubMedCentralCrossRef
Inglis W, Olmstead M, Robbins T (2001a) Selective deficits in atentional performance on the 5-choice serial reaction time task following pedunculopontine tegmental nucleus lesions. Behav Brain Res 123:117–131PubMedCrossRef
Inglis WL, Olmstead MC, Robbins TW (2001b) Selective deficits in attentional performance on the 5-choice serial reaction time task following pedunculopontine tegmental nucleus lesions. Behav Brain Res 123:117–131PubMedCrossRef
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 5:572–577PubMedCrossRef
Janzen J, van‘t Ent D, Lemstra AW, Berendse HW, Barkhof F, Foncke EM (2012) The pedunculopontine nucleus is related to visual hallucinations in Parkinson’s disease: preliminary results of a voxel-based morphometry study. J Neurol 259:147–154PubMedCrossRef
Jellinger KA (1991) Pathology of Parkinson’s disease. Changes other than the nigrostriatal pathway. Mol Chem Neuropathol 14:153–197PubMedCrossRef
Jellinger KA (2012) Neurobiology of cognitive impairment in Parkinson’s disease. Expert Rev Neurother 12:1451–1466PubMedCrossRef
Karachi C, Grabli D, Bernard FA, Tandé D, Wattiez N, Belaid H, Bardinet E, Prigent A, Nothacker HP, Hunot S, Hartmann A, Lehéricy S, Hirsch EC, François C (2010a) Cholinergic mesencephalic neurons are involved in gait and postural disorders in Parkinson disease. J Clin Invest 120:2745–2754PubMedPubMedCentralCrossRef
Karachi C, Grabli D, Bernard FA, Tandé D, Wattiez N, Belaid H, Bardinet E, Prigent A, Nothacker HP, Hunot S, Hartmann A, Lehéricy S, Hirsch EC, François C (2010b) Cholinergic mesencephalic neurons are involved in gait and postural disorders in Parkinson disease. J Clin Invest 120:2745–2754PubMedPubMedCentralCrossRef
Kempster PA, O’Sullivan SS, Holton JL, Revesz T, Lees AJ (2010) Relationships between age and late progression of Parkinson’s disease: a clinico-pathological study. Brain 133:1755–1762PubMedCrossRef
Kessler KR, Ruge D, Ilić TV, Ziemann U (2005) Short latency afferent inhibition and facilitation in patients with writer’s cramp. Mov Disord 20:238–242PubMedCrossRef
Koike T, Kan S, Misaki M, Miyauchi S (2011) Connectivity pattern changes in default-mode network with deep non-REM and REM sleep. Neurosci Res 69:322–330PubMedCrossRef
Kotagal V, Albin RL, Müller ML, Koeppe RA, Chervin RD, Frey KA, Bohnen NI (2012a) Symptoms of rapid eye movement sleep behavior disorder are associated with cholinergic denervation in Parkinson disease. Ann Neurol 71:560–568PubMedPubMedCentralCrossRef
Kotagal V, Albin RL, Müller ML, Koeppe RA, Chervin RD, Frey KA, Bohnen NI (2012b) Symptoms of rapid eye movement sleep behavior disorder are associated with cholinergic denervation in Parkinson disease. Ann Neurol 71:560–568PubMedPubMedCentralCrossRef
Krüger R, Klucken J, Weiss D, Tönges L, Kolber P, Unterecker S, Lorrain M, Baas H, Müller T, Riederer P (2017) Classification of advanced stages of Parkinson’s disease: translation into stratified treatments. J Neural Transm (Vienna) 124:1015–1027CrossRef
Lavoie B, Parent A (1994) Pedunculopontine nucleus in the squirrel monkey: distribution of cholinergic and monoaminergic neurons in the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons. J Comp Neurol 344:190–209PubMedCrossRef
Lee KD, Koo JH, Song SH, Jo KD, Lee MK, Jang W (2015) Central cholinergic dysfunction could be associated with oropharyngeal dysphagia in early Parkinson’s disease. J Neural Transm 122:1553–1561PubMedCrossRef
Lenka A, Hegde S, Jhunjhunwala KR, Pal PK (2016) Interactions of visual hallucinations, rapid eye movement sleep behavior disorder and cognitive impairment in Parkinson’s disease: a review. Park Relat Disord 22:1–8CrossRef
Mahieux F, Fénelon G, Flahault A, Manifacier MJ, Michelet D, Boller F (1998) Neuropsychological prediction of dementia in Parkinson’s disease. J Neurol Neurosurg Psychiatry 64:178–183PubMedPubMedCentralCrossRef
Mandairon N, Ferretti CJ, Stack CM, Rubin DB, Cleland TA, Linster C (2006) Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats. Eur J Neurosci 24:3234–3244PubMedCrossRef
Manford M, Andermann F (1998) Complex visual hallucinations. Clinical and neurobiological insights. Brain 121:1819–1840PubMedCrossRef
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 132:2350–2355PubMedPubMedCentralCrossRef
Martorana A, Mori F, Esposito Z, Kusayanagi H, Monteleone F, Codeca C, Sancesario G, Bernardi G, Koch G (2009) Dopamine modulates cholinergic cortical excitability in Alzheimer’s disease patients. Neuropsychopharmacology 34:2323–2328PubMedCrossRef
Martorana A, Di Lorenzo F, Esposito Z, Lo Giudice T, Bernardi G, Caltagirone C, Koch G (2013) Dopamine D2-agonist Rotigotine effects on cortical excitability and central cholinergic transmission in Alzheimer’s disease patients. Neuropharmacology 64:108–113PubMedCrossRef
Miller N, Noble E, Jones D, Burn D (2006) Hard to swallow: dysphagia in Parkinson’s disease. Age Ageing 35:614–618PubMedCrossRef
Nakano I, Hirano A (1984) Parkinson’s disease: neuron loss in the nucleus basalis without concomitant Alzheimer’s disease. Ann Neurol 15:415–418PubMedCrossRef
Nakano K, Hasegawa Y, Tokushige A, Nakagawa S, Kayahara T, Mizuno N (1990) Topographical projections from the thalamus, subthalamic nucleus and pedunculopontine tegmental nucleus to the striatum in the Japanese monkey, Macaca fuscata. Brain Res 537:54–68PubMedCrossRef
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 163:128–131PubMedCrossRef
Nardone R, Bergmann J, Brigo F, Christova M, Kunz A, Seidl M, Tezzon F, Trinka E, Golaszewski S (2013) Functional evaluation of central cholinergic circuits in patients with Parkinson’s disease and REM sleep behavior disorder: a TMS study. J Neural Transm (Vienna) 20:413–422CrossRef
Nardone R, Höller Y, Thomschewski A, Kunz AB, Lochner P, Golaszewski S, Trinka E, Brigo F (2014) Dopamine differently modulates central cholinergic circuits in patients with Alzheimer disease and CADASIL. J Neural Transm (Vienna) 121:1313–1320CrossRef
Oh E, Park J, Youn J, Kim JS, Park S, Jang W (2017) Olfactory dysfunction in early Parkinson’s disease is associated with short latency afferent inhibition reflecting central cholinergic dysfunction. Clin Neurophysiol 128:1061–1068PubMedCrossRef
Oishi N, Udaka F, Kameyama M, Sawamoto N, Hashikawa K, Fukuyama H (2005) Regional cerebral blood flow in Parkinson disease with nonpsychotic visual hallucinations. Neurology 65:1708–1715PubMedCrossRef
Pahapill PA, Lozano AM (2000) The pedunculopontine nucleus and Parkinson’s disease. Brain 123:1767–1783PubMedCrossRef
Paolini AG, McKenzie JS (1993) Effects of lesions in the horizontal diagonal band nucleus on olfactory habituation in the rat. Neuroscience 57:717–724PubMedCrossRef
Paolini AG, McKenzie JS (1996) Lesions in the magnocellular preoptic nucleus decrease olfactory investigation in rats. Behav Brain Res 81:223–231PubMedCrossRef
Pelosin E, Ogliastro C, Lagravinese G, Bonassi G, Mirelman A, Hausdorff JM, Abbruzzese G, Avanzino L (2016) Attentional control of gait and falls: is cholinergic dysfunction a common substrate in the elderly and Parkinson’s disease? Front Aging Neurosci 8:104PubMedPubMedCentralCrossRef
Perez-Lloret S, Peralta MC, Barrantes FJ (2016) Pharmacotherapies for Parkinson’s disease symptoms related to cholinergic degeneration. Expert Opin Pharmacother 18:2405–2415CrossRef
Perry E, Walker M, Grace J, Perry R (1999) Acetylcholine in mind: a neurotransmitter correlate of consciousness? Trends Neurosci 22:273–280PubMedCrossRef
Picillo M, Dubbioso R, Iodice R, Iavarone A, Pisciotta C, Spina E, Santoro L, Barone P, Amboni M, Manganelli F (2015) Short-latency afferent inhibition in patients with Parkinson’s disease and freezing of gait. J Neural Transm (Vienna) 122:1533–1540CrossRef
Poletti M, Frosini D, Pagni C, Baldacci F, Nicoletti V, Tognoni G, Lucetti C, Del Dotto P, Ceravolo R, Bonuccelli U (2012) Mild cognitive impairment and cognitive-motor relationships in newly diagnosed drug-naive patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 83:601–606PubMedCrossRef
Ravel N, Vigouroux M, Elaagouby A, Gervais R (1992) Scopolamine impairs delayed matching in an olfactory task in rats. Psychopharmacology 109:439–443PubMedCrossRef
Ravel N, Elaagouby A, Gervais R (1994) Scopolamine injection into the olfactory bulb impairs short-term olfactory memory in rats. Behav Neurosci 108:317–324PubMedCrossRef
Richardson SP, Bliem B, Lomarev M, Shamim E, Dang N, Hallett M (2008) Changes in short afferent inhibition during phasic movement in focal dystonia. Muscle Nerve 37:358–363CrossRef
Rizzo V, Aricò I, Mastroeni C, Morgante F, Liotta G, Girlanda P, Silvestri R, Quartarone A (2009) Dopamine agonists restore cortical plasticity in patients with idiopathic restless legs syndrome. Mov Disord 24:710–715PubMedCrossRef
Rochester L, Yarnall AJ, Baker MR, David RV, Lord S, Galna B, Burn DJ (2012) Cholinergic dysfunction contributes to gait disturbance in early Parkinson’s disease. Brain 135(Pt 9):2779–2788PubMedPubMedCentralCrossRef
Rogers JD, Brogan D, Mirra SS (1985) The nucleus basalis of Meynert in neurological disease: a quantitative morphological study. Ann Neurol 17:163–170PubMedCrossRef
Sailer A, Molnar GF, Paradiso G, Gunraj CA, Lang AE, Chen R (2003) Short and long latency afferent inhibition in Parkinson’s disease. Brain 126:1883–1894PubMedCrossRef
Sailer A, Cunic DI, Paradiso GO, Gunraj CA, Wagle-Shukla A, Moro E, Lozano AM, Lang AE, Chen R (2007) Subthalamic nucleus stimulation modulates afferent inhibition in Parkinson disease. Neurology 68:356–363PubMedCrossRef
Santangelo G, Trojano L, Vitale C, Ianniciello M, Amboni M, Grossi D, Barone PA (2007) A neuropsychological longitudinal study in Parkinson’s patients with and without hallucinations. Mov Disord 22:2418–2425PubMedCrossRef
Sarter M, Bruno JP, Turchi J (1999) Basal forebrain afferent projections modulating cortical acetylcholine, attention, and implications for neuropsychiatric disorders. Ann N Y Acad Sci 877:368–382PubMedCrossRef
Shin S, Lee JE, Hong JY, Sunwoo MK, Sohn YH, Lee PH (2012) Neuroanatomical substrates of visual hallucinations in patients with non-demented Parkinson’s disease. J Neurol Neurosurg Psychiatry 83:1155–1161PubMedCrossRef
Stephenson R, Houghton D, Sundararajan SH, Doty RL, Siderowf A, Stern M (2008) Impaired olfaction and subsequent risk of long-term complications of Parkinson’s disease. Mov Disord 23:S282
Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969–1985PubMed
Stiasny-Kolster K, Sixel-Döring F, Trenkwalder C, Heinzel-Gutenbrunner M, Seppi K, Poewe W, Högl B, Frauscher B (2015) Diagnostic value of the REM sleep behavior disorder screening questionnaire in Parkinson’s disease. Sleep Med 16:186–189PubMedCrossRef
Tiraboschi P, Hansen LA, Alford M, Sabbagh MN, Schoos B, Masliah E, Thal LJ, Corey-Bloom J (2000) Cholinergic dysfunction in diseases with Lewy bodies. Neurology 54:407–411PubMedCrossRef
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 523:503–513PubMedPubMedCentralCrossRef
Velayudhan L, Lovestone S (2009) Smell identification test as a treatment response marker in patients with Alzheimer disease receiving donepezil. J Clin Psychopharmacol 29:387–390PubMedCrossRef
Verbaan D, Marinus J, Visser M, van Rooden SM, Stiggelbout AM, Middelkoop HA, van Hilten JJ (2007) Cognitive impairment in Parkinson’s disease. J Neurol Neurosurg Psychiatry 78:1182–1187PubMedPubMedCentralCrossRef
Versace V, Langthaler PB, Sebastianelli L, Höller Y, Brigo F, Orioli A, Saltuari L, Nardone R (2017) Impaired cholinergic transmission in patients with Parkinson’s disease and olfactory dysfunction. J Neurol Sci 377:55–61PubMedCrossRef
Voller B, St Clair Gibson A, Dambrosia J, Pirio Richardson S, Lomarev M, Dang N, Hallett M (2006) Short-latency afferent inhibition during selective finger movement. Exp Brain Res 169:226–231PubMedCrossRef
Whitehouse PJ, Hedreen JC, White CL 3rd, Price DL (1983) Basal forebrain neurons in the dementia of Parkinson disease. Ann Neurol 3:243–248CrossRef
Williams-Gray CH, Foltynie T, Brayne CE, Robbins TW, Barker RA (2007) Evolution of cognitive dysfunction in an incident Parkinson’s disease cohort. Brain 130:1787–1798PubMedCrossRef
Yarnall AJ, Rochester L, Baker MR, David R, Khoo TK, Duncan GW, Galna B, Burn DJ (2013) Short latency afferent inhibition: a biomarker for mild cognitive impairment in Parkinson’s disease? Mov Disord 28:1285–1288PubMedCrossRef
Zarow C, Lyness SA, Mortimer JA, Chui HC (2003) Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 60:337–341PubMedCrossRef
Zweig RM, Jankel WR, Hedreen JC, Mayeux R, Price DL (1989) The pedunculopontine nucleus in Parkinson’s disease. Ann Neurol 26:41–46PubMedCrossRef
Metadata
Title
Cortical afferent inhibition abnormalities reveal cholinergic dysfunction in Parkinson’s disease: a reappraisal
Authors
Raffaele Nardone
Francesco Brigo
Viviana Versace
Yvonne Höller
Frediano Tezzon
Leopold Saltuari
Eugen Trinka
Luca Sebastianelli
Publication date
01-11-2017
Publisher
Springer Vienna
Published in
Journal of Neural Transmission / Issue 11/2017
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-017-1775-y

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