Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Acta Neuropathologica
Published in: Acta Neuropathologica 3/2007

01-09-2007 | Review

Morphological substrate of autonomic failure and neurohormonal dysfunction in multiple system atrophy: impact on determining phenotype spectrum

Author: Tetsutaro Ozawa

Published in: Acta Neuropathologica | Issue 3/2007

Login to get access

Abstract

Autonomic failure is a prominent clinical feature of patients with multiple system atrophy (MSA). Neurohormonal dysfunction is also a frequent accompaniment in patients with MSA. The determination of the pathological involvement of the autonomic neurons, which are responsible for circadian rhythms and responses to stress, provides new insight into autonomic failure and neurohormonal dysfunction in MSA. The disruptions of circadian rhythms and responses to stress may underlie the impairment of homeostatic integration responsible for cardiovascular and respiratory failures. These notions lead to the hypothesis that a pathological involvement of autonomic neurons is a significant factor of the poor prognosis of MSA. Beyond this perspective, endeavors to find the morphological phenotype that represents a predominant loss of autonomic neurons may elucidate the full spectrum of pathological involvements in MSA.
Literature
1.
Andrich J, Schmitz T, Saft C, Postert T, Kraus P, Epplen JT, Przuntek H, Agelink MW (2002) Autonomic nervous system function in Huntington’s disease. J Neurol Neurosurg Psychiatry 72:726–731PubMed
2.
Arai K, Kato N, Kashiwado K, Hattori T (2000) Pure autonomic failure in association with human alpha-synucleinopathy. Neurosci Lett 296:171–173PubMed
3.
Bannister R, Gibson W, Michaels L, Oppenheimer DR (1981) Laryngeal abductor paralysis in multiple system atrophy. A report on three necropsied cases, with observations on the laryngeal muscles and the nuclei ambigui. Brain 104:351–368PubMed
4.
Benarroch EE (2003) Brainstem in multiple system atrophy: clinicopathological correlations. Cell Mol Neurobiol 23:519–526PubMed
5.
Benarroch EE, Schmeichel AM (2001) Depletion of corticotrophin-releasing factor neurons in the pontine micturition area in multiple system atrophy. Ann Neurol 50:640–645PubMed
6.
Benarroch EE, Schmeichel AM, Low PA, Parisi JE (2003) Depletion of ventromedullary NK-1 receptor-immunoreactive neurons in multiple system atrophy. Brain 126:2183–2190PubMed
7.
Benarroch EE, Schmeichel AM, Low PA, Parisi JE (2004) Involvement of medullary serotonergic groups in multiple system atrophy. Ann Neurol 55:418–422PubMed
8.
Benarroch EE, Schmeichel AM, Low PA, Parisi JE (2007) Depletion of putative chemosensitive respiratory neurons in the ventral medullary surface in multiple system atrophy. Brain 130:469–475PubMed
9.
Benarroch EE, Schmeichel AM, Parisi JE (2001) Depletion of cholinergic neurons of the medullary arcuate nucleus in multiple system atrophy. Auton Neurosci 87:293–299PubMed
10.
Benarroch EE, Schmeichel AM, Parisi JE (2003) Preservation of branchimotor neurons of the nucleus ambiguus in multiple system atrophy. Neurology 60:115–117PubMed
11.
Benarroch EE, Schmeichel AM, Sandroni P, Low PA, Parisi JE (2006) Differential involvement of hypothalamic vasopressin neurons in multiple system atrophy. Brain 129:2688–2696PubMed
12.
Benarroch EE, Schmeichel AM, Sandroni P, Low PA, Parisi JE (2006) Involvement of vagal autonomic nuclei in multiple system atrophy and Lewy body disease. Neurology 66:378–383PubMed
13.
Benarroch EE, Schmeichel AM, Sandroni P, Low PA, Parisi JE (2007) Involvement of hypocretin neurons in multiple system atrophy. Acta Neuropathol (Berl) 113:75–80
14.
Benarroch EE, Smithson IL, Low PA, Parisi JE (1998) Depletion of catecholaminergic neurons of the rostral ventrolateral medulla in multiple systems atrophy with autonomic failure. Ann Neurol 43:156–163PubMed
15.
Biaggioni I, Robertson RM (2002) Hypertension in orthostatic hypotension and autonomic dysfunction. Cardiol Clin 20:291–301, viiPubMed
16.
Blessing WW, Willoughby JO (1985) Inhibiting the rabbit caudal ventrolateral medulla prevents baroreceptor-initiated secretion of vasopressin. J Physiol 367:253–265PubMed
17.
Blumin JH, Berke GS (2002) Bilateral vocal fold paresis and multiple system atrophy. Arch Otolaryngol Head Neck Surg 128:1404–1407PubMed
18.
Braak H, Rub U, Del Tredici K (2003) Involvement of precerebellar nuclei in multiple system atrophy. Neuropathol Appl Neurobiol 29:60–76PubMed
19.
Brown RT, Polinsky RJ, Lee GK, Deeter JA (1986) Insulin-induced hypotension and neurogenic orthostatic hypotension. Neurology 36:1402–1406PubMed
20.
Buijs RM, Hermes MH, Kalsbeek A (1998) The suprachiasmatic nucleus-paraventricular nucleus interactions: a bridge to the neuroendocrine and autonomic nervous system. Prog Brain Res 119:365–382PubMed
21.
Buijs RM, la Fleur SE, Wortel J, Van Heyningen C, Zuiddam L, Mettenleiter TC, Kalsbeek A, Nagai K, Niijima A (2003) The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons. J Comp Neurol 464:36–48PubMed
22.
Buijs RM, Wortel J, Van Heerikhuize JJ, Kalsbeek A (1997) Novel environment induced inhibition of corticosterone secretion: physiological evidence for a suprachiasmatic nucleus mediated neuronal hypothalamo-adrenal cortex pathway. Brain Res 758:229–236PubMed
23.
Chandler MP, Mathias CJ (2002) Haemodynamic responses during head-up tilt and tilt reversal in two groups with chronic autonomic failure: pure autonomic failure and multiple system atrophy. J Neurol 249:542–548PubMed
24.
Clarke CE, Ray PS, Speller JM (1999) Failure of the clonidine growth hormone stimulation test to differentiate multiple system atrophy from early or advanced idiopathic Parkinson’s disease. Lancet 353:1329–1330PubMed
25.
Colao A, Marzullo P, Di Somma C, Lombardi G (2001) Growth hormone and the heart. Clin Endocrinol (Oxf) 54:137–154
26.
Cormican LJ, Higgins S, Davidson AC, Howard R, Williams AJ (2004) Multiple system atrophy presenting as central sleep apnoea. Eur Respir J 24:323–325PubMed
27.
Day TA, Sibbald JR (1989) A1 cell group mediates solitary nucleus excitation of supraoptic vasopressin cells. Am J Physiol 257:R1020–R1026PubMed
28.
Deguchi K, Sasaki I, Touge T, Tsukaguchi M, Takeuchi H, Kuriyama S (2004) Abnormal baroreceptor-mediated vasopressin release as possible marker in early diagnosis of multiple system atrophy. J Neurol Neurosurg Psychiatry 75:110–115PubMed
29.
Dotson R, Ochoa J, Marchettini P, Cline M (1990) Sympathetic neural outflow directly recorded in patients with primary autonomic failure: clinical observations, microneurography, and histopathology. Neurology 40:1079–1085PubMed
30.
Freeman ME, Kanyicska B, Lerant A, Nagy G (2000) Prolactin: structure, function, and regulation of secretion. Physiol Rev 80:1523–1631PubMed
31.
Friess E, Kuempfel T, Winkelmann J, Schmid D, Uhr M, Rupprecht R, Holsboer F, Trenkwalder C (2001) Increased growth hormone response to apomorphine in Parkinson disease compared with multiple system atrophy. Arch Neurol 58:241–246PubMed
32.
Fuchs J, Nilsson C, Kachergus J, Munz M, Larsson EM, Schule B, Langston JW, Middleton FA, Ross OA, Hulihan M, Gasser T, Farrer MJ (2007) Phenotypic variation in a large Swedish pedigree due to SNCA duplication and triplication. Neurology
33.
Galassi G, Nemni R, Baraldi A, Gibertoni M, Colombo A (1982) Peripheral neuropathy in multiple system atrophy with autonomic failure. Neurology 32:1116–1121PubMed
34.
Gilman S, Low PA, Quinn N, Albanese A, Ben-Shlomo Y, Fowler CJ, Kaufmann H, Klockgether T, Lang AE, Lantos PL, Litvan I, Mathias CJ, Oliver E, Robertson D, Schatz I, Wenning GK (1999) Consensus statement on the diagnosis of multiple system atrophy. J Neurol Sci 163:94–98PubMed
35.
Gilman S, Sima AA, Junck L, Kluin KJ, Koeppe RA, Lohman ME, Little R (1996) Spinocerebellar ataxia type 1 with multiple system degeneration and glial cytoplasmic inclusions. Ann Neurol 39:241–255PubMed
36.
Glass GA, Josephs KA, Ahlskog JE (2006) Respiratory insufficiency as the primary presenting symptom of multiple-system atrophy. Arch Neurol 63:978–981PubMed
37.
Goldstein DS, Pechnik S, Holmes C, Eldadah B, Sharabi Y (2003) Association between supine hypertension and orthostatic hypotension in autonomic failure. Hypertension 42:136–142PubMed
38.
Graham JG, Oppenheimer DR (1969) Orthostatic hypotension and nicotine sensitivity in a case of multiple system atrophy. J Neurol Neurosurg Psychiatry 32:28–34PubMed
39.
Gray F, Vincent D, Hauw JJ (1988) Quantitative study of lateral horn cells in 15 cases of multiple system atrophy. Acta Neuropathol (Berl) 75:513–518
40.
Gu W, Ma H, Wang K, Jin M, Zhou Y, Liu X, Wang G, Shen Y (2004) The shortest expanded allele of the MJD1 gene in a Chinese MJD kindred with autonomic dysfunction. Eur Neurol 52:107–111PubMed
41.
Hague K, Lento P, Morgello S, Caro S, Kaufmann H (1997) The distribution of Lewy bodies in pure autonomic failure: autopsy findings and review of the literature. Acta Neuropathol (Berl) 94:192–196
42.
Hanson DG, Ludlow CL, Bassich CJ (1983) Vocal fold paresis in Shy-Drager syndrome. Ann Otol Rhinol Laryngol 92:85–90PubMed
43.
Hasen J, Wu RH, Bocsko M (1982) Hypothalamic dysfunction in a case of idiopathic orthostatic hypotension (shy-Drager Syndrome). Am J Med Sci 283:36–40PubMed
44.
Higo R, Tayama N, Watanabe T, Nitou T, Takeuchi S (2003) Vocal fold motion impairment in patients with multiple system atrophy: evaluation of its relationship with swallowing function. J Neurol Neurosurg Psychiatry 74:982–984PubMed
45.
Hirayama M, Fukatsu H, Watanabe H, Koike Y, Noda A, Ito H, Kobayashi R, Sobue G (2003) Sequential constriction of upper airway and vocal cords in sleep apnoea of multiple system atrophy: low field magnetic resonance fluoroscopic study. J Neurol Neurosurg Psychiatry 74:642–645PubMed
46.
Hishikawa N, Hashizume Y, Hirayama M, Imamura K, Washimi Y, Koike Y, Mabuchi C, Yoshida M, Sobue G (2000) Brainstem-type Lewy body disease presenting with progressive autonomic failure and lethargy. Clin Auton Res 10:139–143PubMed
47.
Hofman MA, Purba JS, Swaab DF (1993) Annual variations in the vasopressin neuron population of the human suprachiasmatic nucleus. Neuroscience 53:1103–1112PubMed
48.
Hughes RG, Gibbin KP, Lowe J (1998) Vocal fold abductor paralysis as a solitary and fatal manifestation of multiple system atrophy. J Laryngol Otol 112:177–178PubMed
49.
Isono S, Shiba K, Yamaguchi M, Tanaka A, Hattori T, Konno A, Nishino T (2001) Pathogenesis of laryngeal narrowing in patients with multiple system atrophy. J Physiol 536:237–249PubMed
50.
Isozaki E, Matsubara S, Hayashida T, Oda M, Hirai S (2000) Morphometric study of nucleus ambiguus in multiple system atrophy presenting with vocal cord abductor paralysis. Clin Neuropathol 19:213–220PubMed
51.
Isozaki E, Naito A, Horiguchi S, Kawamura R, Hayashida T, Tanabe H (1996) Early diagnosis and stage classification of vocal cord abductor paralysis in patients with multiple system atrophy. J Neurol Neurosurg Psychiatry 60:399–402PubMed
52.
Jordan J, Biaggioni I (2002) Diagnosis and treatment of supine hypertension in autonomic failure patients with orthostatic hypotension. J Clin Hypertens (Greenwich) 4:139–145
53.
Kanda T, Tsukagoshi H, Oda M, Miyamoto K, Tanabe H (1996) Changes of unmyelinated nerve fibers in sural nerve in amyotrophic lateral sclerosis, Parkinson’s disease and multiple system atrophy. Acta Neuropathol (Berl) 91:145–154
54.
Kaufmann H, Oribe E, Miller M, Knott P, Wiltshire-Clement M, Yahr MD (1992) Hypotension-induced vasopressin release distinguishes between pure autonomic failure and multiple system atrophy with autonomic failure. Neurology 42:590–593PubMed
55.
Kaye JM, Young TM, Mathias CJ, Watson L, Lightman SL (2006) Neuroendocrine and behavioural responses to CO(2) inhalation in central versus peripheral autonomic failure. Clin Auton Res 16:121–129PubMed
56.
Kazuta T, Hayashi M, Shimizu T, Iwasaki A, Nakamura S, Hirai S (2000) Autonomic dysfunction in Machado-Joseph disease assessed by iodine123-labeled metaiodobenzylguanidine myocardial scintigraphy. Clin Auton Res 10:111–115PubMed
57.
Kc P, Haxhiu MA, Tolentino-Silva FP, Wu M, Trouth CO, Mack SO (2002) Paraventricular vasopressin-containing neurons project to brain stem and spinal cord respiratory-related sites. Respir Physiol Neurobiol 133:75–88PubMed
58.
Kennedy PG, Duchen LW (1985) A quantitative study of intermediolateral column cells in motor neuron disease and the Shy-Drager syndrome. J Neurol Neurosurg Psychiatry 48:1103–1106PubMed
59.
Khan NL, Graham E, Critchley P, Schrag AE, Wood NW, Lees AJ, Bhatia KP, Quinn N (2003) Parkin disease: a phenotypic study of a large case series. Brain 126:1279–1292PubMed
60.
Kimber J, Mathias CJ, Lees AJ, Bleasdale-Barr K, Chang HS, Churchyard A, Watson L (2000) Physiological, pharmacological and neurohormonal assessment of autonomic function in progressive supranuclear palsy. Brain 123(Pt 7):1422–1430PubMed
61.
Kimber J, Watson L, Mathias CJ (1999) Neuroendocrine responses to levodopa in multiple system atrophy (MSA). Mov Disord 14:981–987PubMed
62.
Kimber JR, Watson L, Mathias CJ (1997) Distinction of idiopathic Parkinson’s disease from multiple-system atrophy by stimulation of growth-hormone release with clonidine. Lancet 349:1877–1881PubMed
63.
Kitae S, Murata Y, Tachiki N, Okazaki M, Harada T, Nakamura S (2001) Assessment of cardiovascular autonomic dysfunction in multiple system atrophy. Clin Auton Res 11:39–44PubMed
64.
Kneisley LW, Rederich GJ (1990) Nocturnal stridor in olivopontocerebellar atrophy. Sleep 13:362–368PubMed
65.
Kollensperger M, Stampfer-Kountchev M, Seppi K, Geser F, Frick C, Del Sorbo F, Albanese A, Gurevich T, Giladi N, Djaldetti R, Schrag A, Low PA, Mathias CJ, Poewe W, Wenning GK (2007) Progression of dysautonomia in multiple system atrophy: a prospective study of self-perceived impairment. Eur J Neurol 14:66–72PubMed
66.
Konno H, Yamamoto T, Iwasaki Y, Iizuka H (1986) Shy-Drager syndrome and amyotrophic lateral sclerosis. Cytoarchitectonic and morphometric studies of sacral autonomic neurons. J Neurol Sci 73:193–204PubMed
67.
Lee EA, Kim BJ, Lee WY (2002) Diagnosing multiple system atrophy with greater accuracy: combined analysis of the clonidine-growth hormone test and external anal sphincter electromyography. Mov Disord 17:1242–1247PubMed
68.
Lin IS, Wu RM, Lee-Chen GJ, Shan DE, Gwinn-Hardy K (2007) The SCA17 phenotype can include features of MSA-C, PSP and cognitive impairment. Parkinsonism Relat Disord 13:246–249PubMed
69.
Low PA, Thomas JE, Dyck PJ (1978) The splanchnic autonomic outflow in Shy-Drager syndrome and idiopathic orthostatic hypotension. Ann Neurol 4:511–514PubMed
70.
Ludwig M, Horn T, Callahan MF, Grosche A, Morris M, Landgraf R (1994) Osmotic stimulation of the supraoptic nucleus: central and peripheral vasopressin release and blood pressure. Am J Physiol 266:E351–E356PubMed
71.
Mabuchi N, Hirayama M, Koike Y, Watanabe H, Ito H, Kobayashi R, Hamada K, Sobue G (2005) Progression and prognosis in pure autonomic failure (PAF): comparison with multiple system atrophy. J Neurol Neurosurg Psychiatry 76:947–952PubMed
72.
Magalhaes M, Wenning GK, Daniel SE, Quinn NP (1995) Autonomic dysfunction in pathologically confirmed multiple system atrophy and idiopathic Parkinson’s disease—a retrospective comparison. Acta Neurol Scand 91:98–102PubMedCrossRef
73.
Mannen T (1991) Neuropathology of Onuf’s nucleus. Rinsho Shinkeigaku 31:1281–1285PubMed
74.
Mannen T, Iwata M, Toyokura Y, Nagashima K (1982) The Onuf’s nucleus and the external anal sphincter muscles in amyotrophic lateral sclerosis and Shy-Drager syndrome. Acta Neuropathol (Berl) 58:255–260
75.
Mathias CJ (1997) Autonomic disorders and their recognition. N Engl J Med 336:721–724PubMed
76.
Mathias CJ, Fosbraey P, da Costa DF, Thornley A, Bannister R (1986) The effect of desmopressin on nocturnal polyuria, overnight weight loss, and morning postural hypotension in patients with autonomic failure. Br Med J (Clin Res Ed) 293:353–354
77.
Mathias CJ, Mallipeddi R, Bleasdale-Barr K (1999) Symptoms associated with orthostatic hypotension in pure autonomic failure and multiple system atrophy. J Neurol 246:893–898PubMed
78.
Merlo IM, Occhini A, Pacchetti C, Alfonsi E (2002) Not paralysis, but dystonia causes stridor in multiple system atrophy. Neurology 58:649–652PubMed
79.
Mochizuki A, Mizusawa H, Ohkoshi N, Yoshizawa K, Komatsuzaki Y, Inoue K, Kanazawa I (1992) Argentophilic intracytoplasmic inclusions in multiple system atrophy. J Neurol 239:311–316PubMed
80.
Moore RY (1997) Circadian rhythms: basic neurobiology and clinical applications. Annu Rev Med 48:253–266PubMed
81.
Moore RY, Eichler VB (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42:201–206PubMed
82.
Nakamura S, Ohnishi K, Nishimura M, Suenaga T, Akiguchi I, Kimura J, Kimura T (1996) Large neurons in the tuberomammillary nucleus in patients with Parkinson’s disease and multiple system atrophy. Neurology 46:1693–1696PubMed
83.
Nishie M, Mori F, Fujiwara H, Hasegawa M, Yoshimoto M, Iwatsubo T, Takahashi H, Wakabayashi K (2004) Accumulation of phosphorylated alpha-synuclein in the brain and peripheral ganglia of patients with multiple system atrophy. Acta Neuropathol (Berl) 107:292–298
84.
Noda K, Katayama S, Watanabe C, Yamamura Y, Nakamura S (1997) Decrease of neurons in the medullary arcuate nucleus of multiple system atrophy: quantitative comparison with Parkinson’s disease and amyotrophic lateral sclerosis. J Neurol Sci 151:89–91PubMed
85.
Noda K, Katayama S, Watanabe C, Yamamura Y, Nakamura S, Yonehara S, Inai K (1996) Pure autonomic failure with motor neuron disease: report of a clinical study and postmortem examination of a patient. J Neurol Neurosurg Psychiatry 60:351–352PubMed
86.
Nomura H, Konno H, Takase S, Saito H (2001) Decrease of substance P in the parabrachial nucleus of multiple system atrophy. Auton Neurosci 92:86–91PubMed
87.
Norbiato G, Bevilacqua M, Righini V, Chebat E, Vago T, Bertora P, Castelli L, Mangoni A (1992) Altered vasopressin response to metoclopramide in multiple system atrophy: evidence of a cholinergic defect in the hypothalamus. Acta Neurol Scand 85:299–303PubMedCrossRef
88.
Oppenheimer DR (1980) Lateral horn cells in progressive autonomic failure. J Neurol Sci 46:393–404PubMed
89.
Orimo S, Amino T, Itoh Y, Takahashi A, Kojo T, Uchihara T, Tsuchiya K, Mori F, Wakabayashi K, Takahashi H (2005) Cardiac sympathetic denervation precedes neuronal loss in the sympathetic ganglia in Lewy body disease. Acta Neuropathol (Berl) 109:583–588
90.
Orimo S, Kanazawa T, Nakamura A, Uchihara T, Mori F, Kakita A, Wakabayashi K, Takahashi H (2007) Degeneration of cardiac sympathetic nerve can occur in multiple system atrophy. Acta Neuropathol (Berl) 113:81–86
91.
Oyanagi K, Wakabayashi K, Ohama E, Takeda S, Horikawa Y, Morita T, Ikuta F (1990) Lewy bodies in the lower sacral parasympathetic neurons of a patient with Parkinson’s disease. Acta Neuropathol (Berl) 80:558–559
92.
Ozawa T (2006) Pathology and genetics of multiple system atrophy: an approach to determining genetic susceptibility spectrum. Acta Neuropathol (Berl) 112:531–538
93.
Ozawa T, Oyanagi K, Tanaka H, Horikawa Y, Takahashi H, Morita T, Tsuji S (1998) Suprachiasmatic nucleus in a patient with multiple system atrophy with abnormal circadian rhythm of arginine-vasopressin secretion into plasma. J Neurol Sci 154:116–121PubMed
94.
Ozawa T, Paviour D, Quinn NP, Josephs KA, Sangha H, Kilford L, Healy DG, Wood NW, Lees AJ, Holton JL, Revesz T (2004) The spectrum of pathological involvement of the striatonigral and olivopontocerebellar systems in multiple system atrophy: clinicopathological correlations. Brain 127:2657–2671PubMed
95.
Ozawa T, Soma Y, Yoshimura N, Fukuhara N, Tanaka M, Tsuji S (2001) Reduced morning cortisol secretion in patients with multiple system atrophy. Clin Auton Res 11:271–272PubMed
96.
Ozawa T, Tanaka H, Miyatake T, Tsuji S (1993) Shy-Drager syndrome with abnormal circadian rhythm of plasma antidiuretic hormone secretion and urinary excretion. Intern Med 32:225–227PubMed
97.
Ozawa T, Tanaka H, Nakano R, Sato M, Inuzuka T, Soma Y, Yoshimura N, Fukuhara N, Tsuji S (1999) Nocturnal decrease in vasopressin secretion into plasma in patients with multiple system atrophy. J Neurol Neurosurg Psychiatry 67:542–545PubMed
98.
Parikh SM, Diedrich A, Biaggioni I, Robertson D (2002) The nature of the autonomic dysfunction in multiple system atrophy. J Neurol Sci 200:1–10PubMed
99.
Pavy-Le Traon A, Hughson RL, Thalamas C, Galitsky M, Fabre N, Rascol O, Senard JM (2006) Cerebral autoregulation is preserved in multiple system atrophy: a transcranial Doppler study. Mov Disord 21:2122–2126PubMed
100.
Pazo JH, Belforte JE (2002) Basal ganglia and functions of the autonomic nervous system. Cell Mol Neurobiol 22:645–654PubMed
101.
Pellecchia MT, Longo K, Pivonello R, Lucetti C, Marchese R, Spampani A, Manfredi M, Epifanio A, Sensi M, Scaravilli T, Bracco F, Eleopra R, Morgante L, Donati E, Marconi R, Abbruzzese G, Bonuccelli U, Zappia M, Colao A, Barone P (2006) Multiple system atrophy is distinguished from idiopathic Parkinson’s disease by the arginine growth hormone stimulation test. Ann Neurol 60:611–615PubMed
102.
Pellecchia MT, Pivonello R, Salvatore E, Faggiano A, Barone P, De Michele G, Lombardi G, Colao A, Filla A (2005) Growth hormone response to arginine test distinguishes multiple system atrophy from Parkinson’s disease and idiopathic late-onset cerebellar ataxia. Clin Endocrinol (Oxf) 62:428–433
103.
Pierangeli G, Provini F, Maltoni P, Barletta G, Contin M, Lugaresi E, Montagna P, Cortelli P (2001) Nocturnal body core temperature falls in Parkinson’s disease but not in Multiple-System Atrophy. Mov Disord 16:226–232PubMed
104.
Plaschke M, Trenkwalder P, Dahlheim H, Lechner C, Trenkwalder C (1998) Twenty-four-hour blood pressure profile and blood pressure responses to head-up tilt tests in Parkinson’s disease and multiple system atrophy. J Hypertens 16:1433–1441PubMed
105.
Polinsky RJ, Brown RT, Lee GK, Timmers K, Culman J, Foldes O, Kopin IJ, Recant L (1987) Beta-endorphin, ACTH, and catecholamine responses in chronic autonomic failure. Ann Neurol 21:573–577PubMed
106.
Puritz R, Lightman SL, Wilcox CS, Forsling M, Bannister R (1983) Blood pressure and vasopressin in progressive autonomic failure. Response to postural stimulation, L-dopa and naloxone. Brain 106(Pt 2):503–511PubMed
107.
Pyner S, Coote JH (2000) Identification of branching paraventricular neurons of the hypothalamus that project to the rostroventrolateral medulla and spinal cord. Neuroscience 100:549–556PubMed
108.
Quinn N (1989) Multiple system atrophy–the nature of the beast. J Neurol Neurosurg Psychiatry Suppl:78–89
109.
Ranson RN, Motawei K, Pyner S, Coote JH (1998) The paraventricular nucleus of the hypothalamus sends efferents to the spinal cord of the rat that closely appose sympathetic preganglionic neurones projecting to the stellate ganglion. Exp Brain Res 120:164–172PubMed
110.
Reyes BA, Valentino RJ, Xu G, Van Bockstaele EJ (2005) Hypothalamic projections to locus coeruleus neurons in rat brain. Eur J Neurosci 22:93–106PubMed
111.
Ruggiero DA, Cravo SL, Arango V, Reis DJ (1989) Central control of the circulation by the rostral ventrolateral reticular nucleus: anatomical substrates. Prog Brain Res 81:49–79PubMedCrossRef
112.
Sadaoka T, Kakitsuba N, Fujiwara Y, Kanai R, Takahashi H (1996) Sleep-related breathing disorders in patients with multiple system atrophy and vocal fold palsy. Sleep 19:479–484PubMed
113.
Sage D, Maurel D, Bosler O (2001) Involvement of the suprachiasmatic nucleus in diurnal ACTH and corticosterone responsiveness to stress. Am J Physiol Endocrinol Metab 280:E260–E269PubMed
114.
Sakajiri K, Makifuchi T, Fukuhara N, Nakajima T (1996) Quantitative study of intermediolateral column cell counts in Machado-Joseph disease. J Neurol Sci 144:156–159PubMed
115.
Sakakibara R, Hattori T, Uchiyama T, Kita K, Asahina M, Suzuki A, Yamanishi T (2000) Urinary dysfunction and orthostatic hypotension in multiple system atrophy: which is the more common and earlier manifestation? J Neurol Neurosurg Psychiatry 68:65–69PubMed
116.
Sakakibara R, Uchida Y, Uchiyama T, Yamanishi T, Hattori T (2004) Reduced cerebellar vermis activation during urinary storage and micturition in multiple system atrophy: 99mTc-labelled ECD SPECT study. Eur J Neurol 11:705–708PubMed
117.
Saper CB (1998) “All fall down”: the mechanism of orthostatic hypotension in multiple systems atrophy and Parkinson’s disease. Ann Neurol 43:149–151PubMed
118.
Sasaki K, Aoyagi K, Murabayashi S, Baba T, Kitaoka M, Mastunaga M, Takebe K (1983) Pituitary-adrenocortical system in patients with Shy-Drager syndrome. Horm Metab Res 15:143–146PubMed
119.
Sasaki K, Matsuhashi A, Murabayashi S, Aoyagi K, Baba T, Matsunaga M, Takebe K (1983) Hormonal response to insulin-induced hypoglycemia in patients with Shy-Drager syndrome. Metabolism 32:977–981PubMed
120.
Sawchenko PE, Swanson LW (1981) Central noradrenergic pathways for the integration of hypothalamic neuroendocrine and autonomic responses. Science 214:685–687PubMed
121.
Schwartz WJ, Reppert SM (1985) Neural regulation of the circadian vasopressin rhythm in cerebrospinal fluid: a pre-eminent role for the suprachiasmatic nuclei. J Neurosci 5:2771–2778PubMed
122.
Shimohata T, Nakayama H, Shinoda H, Tsukada H, Takahashi S, Gejo F, Nishizawa M (2006) Multiple system atrophy with progressive nocturnal hypoxemia: case report with polysomnography and continuous positive airway pressure treatment. Eur Neurol 56:258–260PubMed
123.
Shimohata T, Shinoda H, Nakayama H, Ozawa T, Terajima K, Yoshizawa H, Matsuzawa Y, Onodera O, Naruse S, Tanaka K, Takahashi S, Gejyo F, Nishizawa M (2007) Daytime hypoxemia, sleep-disordered breathing and laryngopharyngeal findings in multiple system atrophy. Arch Neurol 64:856–861PubMed
124.
Simpson DM, Kaufmann H, Sanders I, Wolfe DE (1992) Laryngeal dystonia in multiple system atrophy. Muscle Nerve 15:1213–1215PubMed
125.
Singleton A, Gwinn-Hardy K, Sharabi Y, Li ST, Holmes C, Dendi R, Hardy J, Singleton A, Crawley A, Goldstein DS (2004) Association between cardiac denervation and parkinsonism caused by alpha-synuclein gene triplication. Brain 127:768–772PubMed
126.
Sladek CD (2004) Vasopressin response to osmotic and hemodynamic stress: neurotransmitter involvement. Stress 7:85–90PubMed
127.
Sobue G, Hashizume Y, Ohya M, Takahashi A (1986) Shy-Drager syndrome: neuronal loss depends on size, function, and topography in ventral spinal outflow. Neurology 36:404–407PubMed
128.
Sone M, Yoshida M, Hashizume Y, Hishikawa N, Sobue G (2005) alpha-Synuclein-immunoreactive structure formation is enhanced in sympathetic ganglia of patients with multiple system atrophy. Acta Neuropathol (Berl) 110:19–26
129.
Stephan FK, Zucker I (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 69:1583–1586PubMed
130.
Suzuki A, Asahina M, Ishikawa C, Asahina KM, Honma K, Fukutake T, Hattori T (2005) Impaired circadian rhythm of gastric myoelectrical activity in patients with multiple system atrophy. Clin Auton Res 15:368–372PubMed
131.
Swaab DF, Fliers E, Partiman TS (1985) The suprachiasmatic nucleus of the human brain in relation to sex, age and senile dementia. Brain Res 342:37–44PubMed
132.
Tada M, Onodera O, Tada M, Ozawa T, Piao YS, Kakita A, Takahashi H, Nishizawa M (2007) Early development of autonomic dysfunction may predict poor prognosis in patients with multiple system atrophy. Arch Neurol 64:256–260PubMed
133.
Thomaides T, Bleasdale-Barr K, Chaudhuri KR, Pavitt D, Marsden CD, Mathias CJ (1993) Cardiovascular and hormonal responses to liquid food challenge in idiopathic Parkinson’s disease, multiple system atrophy, and pure autonomic failure. Neurology 43:900–904PubMed
134.
Thomaides TN, Chaudhuri KR, Maule S, Watson L, Marsden CD, Mathias CJ (1992) Growth hormone response to clonidine in central and peripheral primary autonomic failure. Lancet 340:263–266PubMed
135.
Tohgi H, Tabuchi M, Tomonaga M, Izumiyama N (1982) Selective loss of small myelinated and unmyelinated fibers in Shy-Drager syndrome. Acta Neuropathol (Berl) 57:282–286
136.
Tomonaga M (1983) Neuropathology of the locus ceruleus: a semi-quantitative study. J Neurol 230:231–240PubMed
137.
Torner L, Neumann ID (2002) The brain prolactin system: involvement in stress response adaptations in lactation. Stress 5:249–257PubMedCrossRef
138.
Tranchant C, Guiraud-Chaumeil C, Echaniz-Laguna A, Warter JM (2000) Is clonidine growth hormone stimulation a good test to differentiate multiple system atrophy from idiopathic Parkinson’s disease? J Neurol 247:853–856PubMed
139.
Tsai A, Maehara K, Iizuka R (1992) Loss of catecholaminergic neuron in the hypothalamus of multiple system atrophy. Rinsho Shinkeigaku 32:125–130PubMed
140.
Tsuda T, Onodera H, Okabe S, Kikuchi Y, Itoyama Y (2002) Impaired chemosensitivity to hypoxia is a marker of multiple system atrophy. Ann Neurol 52:367–371PubMed
141.
Uzawa A, Sakakibara R, Tamura N, Asahina M, Yamanaka Y, Uchiyama T, Ito T, Yamamoto T, Liu Z, Hattori T (2005) Laryngeal abductor paralysis can be a solitary manifestation of multiple system atrophy. J Neurol Neurosurg Psychiatry 76:1739–1741PubMed
142.
Valentino RJ, Foote SL, Page ME (1993) The locus coeruleus as a site for integrating corticotropin-releasing factor and noradrenergic mediation of stress responses. Ann N Y Acad Sci 697:173–188PubMed
143.
van Ingelghem E, van Zandijcke M, Lammens M (1994) Pure autonomic failure: a new case with clinical, biochemical, and necropsy data. J Neurol Neurosurg Psychiatry 57:745–747PubMed
144.
Voisin DL, Chakfe Y, Bourque CW (1999) Coincident detection of CSF Na+ and osmotic pressure in osmoregulatory neurons of the supraoptic nucleus. Neuron 24:453–460PubMed
145.
Wakabayashi K, Takahashi H (1997) Neuropathology of autonomic nervous system in Parkinson’s disease. Eur Neurol 38(Suppl 2):2–7PubMed
146.
Wakabayashi K, Takahashi H, Ohama E, Ikuta F (1990) Parkinson’s disease: an immunohistochemical study of Lewy body-containing neurons in the enteric nervous system. Acta Neuropathol (Berl) 79:581–583
147.
Wakabayashi K, Takahashi H, Ohama E, Takeda S, Ikuta F (1993) Lewy bodies in the visceral autonomic nervous system in Parkinson’s disease. Adv Neurol 60:609–612PubMed
148.
Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F (1988) Parkinson’s disease: the presence of Lewy bodies in Auerbach’s and Meissner’s plexuses. Acta Neuropathol (Berl) 76:217–221
149.
Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F (1989) Lewy bodies in the enteric nervous system in Parkinson’s disease. Arch Histol Cytol 52(Suppl):191–194PubMed
150.
Watanabe H, Saito Y, Terao S, Ando T, Kachi T, Mukai E, Aiba I, Abe Y, Tamakoshi A, Doyu M, Hirayama M, Sobue G (2002) Progression and prognosis in multiple system atrophy: an analysis of 230 Japanese patients. Brain 125:1070–1083PubMed
151.
Wenning GK, Ben Shlomo Y, Magalhaes M, Daniel SE, Quinn NP (1994) Clinical features and natural history of multiple system atrophy. An analysis of 100 cases. Brain 117(Pt 4):835–845PubMed
152.
Wenning GK, Quinn N, Magalhaes M, Mathias C, Daniel SE (1994) “Minimal change” multiple system atrophy. Mov Disord 9:161–166PubMed
153.
Williams TD, Lightman SL, Bannister R (1985) Vasopressin secretion in progressive autonomic failure: evidence for defective afferent cardiovascular pathways. J Neurol Neurosurg Psychiatry 48:225–228PubMedCrossRef
154.
Winkler AS, Landau S, Chaudhuri KR (2002) Serum prolactin levels in Parkinson’s disease and multiple system atrophy. Clin Auton Res 12:393–398PubMed
155.
Wu YR, Chen CM, Ro LS, Chen ST, Tang LM (1996) Vocal cord paralysis as an initial sign of multiple system atrophy in the central nervous system. J Formos Med Assoc 95:804–806PubMed
156.
Yamada M, Hayashi S, Tsuji S, Takahashi H (2001) Involvement of the cerebral cortex and autonomic ganglia in Machado-Joseph disease. Acta Neuropathol (Berl) 101:140–144
157.
Yeh TH, Lu CS, Chou YH, Chong CC, Wu T, Han NH, Chen RS (2005) Autonomic dysfunction in Machado-Joseph disease. Arch Neurol 62:630–636PubMed
158.
Yoshida K, Tashiro K, Matsumoto A, Maruo Y, Hamada K, Hamada T, Doi S (1987) An autopsy case of Shy-Drager syndrome preceded by a urinary disturbance for over 20 years. No To Shinkei 39:59–64PubMed
159.
Zoukos Y, Thomaides T, Pavitt DV, Cuzner ML, Mathias CJ (1993) Beta-adrenoceptor expression on circulating mononuclear cells of idiopathic Parkinson’s disease and autonomic failure patients before and after reduction of central sympathetic outflow by clonidine. Neurology 43:1181–1187PubMed
Metadata
Title
Morphological substrate of autonomic failure and neurohormonal dysfunction in multiple system atrophy: impact on determining phenotype spectrum
Author
Tetsutaro Ozawa
Publication date
01-09-2007
Publisher
Springer-Verlag
Published in
Acta Neuropathologica / Issue 3/2007
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-007-0254-1

Other articles of this Issue 3/2007

Acta Neuropathologica 3/2007 Go to the issue

Original Paper

Co-morbidity of TDP-43 proteinopathy in Lewy body related diseases

Editorial

Announcing the winner of the 2007 Kurt Jellinger Prize

Announcements

Kurt Jellinger Prize 2008 for Outstanding Scientific Writing in Neuropathology

Original Paper

Morphological and biochemical characterisation of sensory neurons infected in vitro with rabies virus

Original Paper

Lrrk2 and chronic inflammation are linked to pallido-ponto-nigral degeneration caused by the N279K tau mutation

Case Report

Lewy body dysphagia