Pedunculopontine cholinergic cell loss in hallucinating Parkinson disease patients but not in dementia with Lewy bodies patients

Journal of Neuropathology and Experimental Neurology

Volumn 72, Issue 12, 2013, Pages 1162-1170

  Hepp, Dagmar Hyacintha ^a,b   Ruiter, A M ^b   Galis, Y ^a   Voorn, P ^a   Rozemuller, A J M ^c   Berendse, H W ^b   Foncke, E M J ^b   Van De Berg, W D J ^a  

^a Department of Anatomy and Neurosciences   (United States)

^b Department of Neurology ^*  (United States)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Acetylcholine; Dementia with Lewy bodies; Parkinson disease; Parkinson disease with dementia; Pedunculopontine tegmental nucleus; Visual hallucinations

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN;

AGED; ALZHEIMER DISEASE; AMYLOID PLAQUE; ARTICLE; AUTOPSY; BRAIN STEM; BRAIN TISSUE; CELL DENSITY; CELL LOSS; CHOLINERGIC ACTIVITY; CHOLINERGIC NERVE CELL; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DIFFUSE LEWY BODY DISEASE; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; MALE; MORPHOMETRICS; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; PARKINSON DISEASE; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PRIORITY JOURNAL; VISUAL HALLUCINATION;

AGED; AMYLOID BETA-PEPTIDES; CELL DEATH; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC NEURONS; FEMALE; HALLUCINATIONS; HUMANS; LEWY BODY DISEASE; MALE; MIDDLE AGED; PARKINSON DISEASE; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; POSTMORTEM CHANGES; STATISTICS, NONPARAMETRIC;

EID: 84889103053     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0000000000000014     Document Type: Article

References (50)

1. McKeith IG, Dickson DW, Lowe J, et al. Diagnosis and management of dementia with Lewy bodies: Third report of the DLB Consortium. Neurology 2005;65:1863-72 (Pubitemid 43970103)
2. Aarsland D, Ballard CG, Halliday G. Are Parkinson's disease with dementia and dementia with Lewy bodies the same entity? J Geriatr Psychiatry Neurol 2004;17:137-45 (Pubitemid 39128223)
3. Bohnen NI, Albin RL. The cholinergic system and Parkinson disease. Behav Brain Res 2011;221:564-73
4. Francis PT, Perry EK. Cholinergic and other neurotransmitter mechanisms in Parkinson's disease, Parkinson's disease dementia, and dementia with Lewy bodies. Mov Disord 2007;22(Suppl 17):S351-57 (Pubitemid 350134188)
5. Bohnen NI, Muller ML, Kotagal V, et al. Heterogeneity of cholinergic denervation in Parkinson's disease without dementia. J Cereb Blood Flow Metab 2012;32:1609-17
6. Kotagal V, Albin RL, Muller ML, et al. Symptoms of rapid eye movement sleep behavior disorder are associated with cholinergic denervation in Parkinson disease. Ann Neurol 2012;71:560-68
7. Marra C, Quaranta D, Profice P, et al. Central cholinergic dysfunction measured "in vivo" correlates with different behavioral disorders in Alzheimer's disease and dementia with Lewy body. Brain Stimul 2012;5: 533-38
8. Yarnall A, Rochester L, Burn DJ. The interplay of cholinergic function, attention, and falls in Parkinson's disease. Mov Disord 2011;26: 2496-503
9. Onofrj M, Taylor JP, Monaco D, et al. Visual Hallucinations in PD and Lewy body dementias: Old and new hypotheses. Behav Neurol 2012 [Epub ahead of print]
10. Sofroniew MV, Priestley JV, Consolazione A, et al. Cholinergic projections from the midbrain and pons to the thalamus in the rat, identified by combined retrograde tracing and choline acetyltransferase immunohistochemistry. Brain Res 1985;329:213-23 (Pubitemid 15142236)
11. Lavoie B, Parent A. Pedunculopontine nucleus in the squirrel monkey: Projections to the basal ganglia as revealed by anterograde tract-tracing methods. J Comp Neurol 1994;344:210-31 (Pubitemid 24151190)
12. Garcia-Rill E. The pedunculopontine nucleus. Prog Neurobiol 1991;36: 363-89
13. Benarroch EE. Pedunculopontine nucleus: Functional organization and clinical implications. Neurology 2013;80:1148-55
14. Olszewski J, Baxter DW. Cytoarchitecture of the human brain stem. Anat Rec 1953;115:435
15. Mesulam MM, Geula C, Bothwell MA, et al. Human reticular formation: Cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons. J Comp Neurol 1989;283:611-33 (Pubitemid 19193471)
16. Pahapill PA, Lozano AM. The pedunculopontine nucleus and Parkinson's disease. Brain 2000;123:1767-83 (Pubitemid 30664282)
17. Dugger BN, Murray ME, Boeve BF, et al. Neuropathological analysis of brainstem cholinergic and catecholaminergic nuclei in relation to rapid eye movement (REM) sleep behaviour disorder. Neuropathol Appl Neurobiol 2012;38:142-52
18. Schmeichel AM, Buchhalter LC, Low PA, et al. Mesopontine cholinergic neuron involvement in Lewy body dementia and multiple system atrophy. Neurology 2008;70:368-73 (Pubitemid 351653399)
19. Daniel SE, Lees AJ. Parkinson's Disease Society Brain Bank, London: Overview and research. J Neural Transm Suppl 1993;39:165-72 (Pubitemid 23216938)
20. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991;82:239-59
21. Selikhova M, Williams DR, Kempster PA, et al. A clinico-pathological study of subtypes in Parkinson's disease. Brain 2009;132:2947-57
22. Olde Dubbelink KT, Stoffers D, Deijen JB, et al. Cognitive decline in Parkinson's disease is associated with slowing of resting-state brain activity: A longitudinal study. Neurobiol Aging 2013;34:408-18
23. Braak H, Del Tredici K, Rüb U, et al. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003;24:197-211 (Pubitemid 36007810)
24. Mirra SS, Heyman A, McKeel D, et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991; 41:479-86
25. Thal DR, Rüb U, Schultz C, et al. Sequence of Abeta-protein deposition in the human medial temporal lobe. J Neuropathol Exp Neurol 2000;59: 733-48 (Pubitemid 30626743)
26. Paxinos G. Human Brain Stem Atlas. San Diego, CA: Academic Press, 1995
27. van Dijk KD, Berendse HW, Drukarch B, et al. The proteome of the locus ceruleus in Parkinson's disease: Relevance to pathogenesis. Brain Pathol 2012;22:485-98
28. Schmitz C, Hof PR. Design-based stereology in neuroscience. Neuroscience 2005;130:813-31 (Pubitemid 40094616)
29. West MJ. Stereological methods for estimating the total number of neurons and synapses: Issues of precision and bias. Trends Neurosci 1999;22:51-61 (Pubitemid 29125550)
30. Alafuzoff I, Ince PG, Arzberger T, et al. Staging/typing of Lewy body Yrelated alpha-synuclein pathology: A study of the Brain Net Europe Consortium. Acta Neuropathol 2009;117:635-52
31. Alafuzoff I, Arzberger T, Al-Sarraj S, et al. Staging of neurofibrillary pathology in Alzheimer's disease: A study of the BrainNet Europe Consortium. Brain Pathol 2008;18:484-96
32. Zweig RM, Jankel WR, Hedreen JC, et al. The pedunculopontine nucleus in Parkinson's disease. Ann Neurol 1989;26:41-46 (Pubitemid 19190041)
33. Hirsch EC, Graybiel AM, Duyckaerts C, et al. Neuronal loss in the pedunculopontine tegmental nucleus in Parkinson disease and in progressive supranuclear palsy. Proc Natl Acad Sci U S A 1987;84:5976-80 (Pubitemid 17135731)
34. Jellinger K. The pedunculopontine nucleus in Parkinson's disease, progressive supranuclear palsy and Alzheimer's disease. J Neurol Neurosurg Psychiatry 1988;51:540-43
35. Rinne JO, Ma SY, Lee MS, et al. Loss of cholinergic neurons in the pedunculopontine nucleus in Parkinson's disease is related to disability of the patients. Parkinsonism Relat Disord 2008;14:553-57
36. Gallagher DA, Parkkinen L, O'Sullivan SS, et al. Testing an aetiological model of visual hallucinations in Parkinson's disease. Brain 2011;134: 3299-309
37. Diederich NJ, Goetz CG, Stebbins GT. Repeated visual hallucinations in Parkinson's disease as disturbed external/internal perceptions: Focused review and a new integrative model. Mov Disord 2005;20:130-40 (Pubitemid 40361115)
38. Collerton D, Perry E, McKeith I. Why people see things that are not there: A novel perception and attention deficit model for recurrent complex visual hallucinations. Behav Brain Sci 2005;28:737-57 (Pubitemid 43372762)
39. Diederich NJ, Fenelon G, Stebbins G, et al. Hallucinations in Parkinson disease. Nat Rev Neurol 2009;5:331-42
40. Mena-Segovia J, Bolam JP, Magill PJ. Pedunculopontine nucleus and basal ganglia: Distant relatives or part of the same family? Trends Neurosci 2004;27:585-88 (Pubitemid 39221393)
41. Bohnen NI, Muller ML, Koeppe RA, et al. History of falls in Parkinson disease is associated with reduced cholinergic activity. Neurology 2009; 73:1670-76
42. Ziabreva I, Ballard CG, Aarsland D, et al. Lewy body disease: Thalamic cholinergic activity related to dementia and parkinsonism. Neurobiol Aging 2006;27:433-38 (Pubitemid 43185328)
43. Perry EK, Marshall E, Kerwin J, et al. Evidence of a monoaminergiccholinergic imbalance related to visual hallucinations in Lewy body dementia. J Neurochem 1990;55:1454-56
44. Tiraboschi P, Hansen LA, Alford M, et al. Early and widespread cholinergic losses differentiate dementia with Lewy bodies from Alzheimer disease. Arch Gen Psychiatry 2002;59:946-51
45. Lippa CF, Smith TW, Perry E. Dementia with Lewy bodies: Choline acetyltransferase parallels nucleus basalis pathology. J Neural Transm 1999;106:525-35 (Pubitemid 29273890)
46. Janzen J, van 't ED, Lemstra AW, et al. The pedunculopontine nucleus is related to visual hallucinations in Parkinson's disease: Preliminary results of a voxel-based morphometry study. J Neurol 2012;259:147-54
47. Dickson DW, Braak H, Duda JE, et al. Neuropathological assessment of Parkinson's disease: Refining the diagnostic criteria. Lancet Neurol 2009;8:1150-57
48. Marques O, Outeiro TF. Alpha-synuclein: From secretion to dysfunction and death. Cell Death Dis 2012;3:e350
49. Jellinger KA, Attems J. Does striatal pathology distinguish Parkinson disease with dementia and dementia with Lewy bodies? Acta Neuropathol 2006;112:253-60 (Pubitemid 44275880)
50. Halliday GM, Song YJ, Harding AJ. Striatal beta-amyloid in dementia with Lewy bodies but not Parkinson's disease. J Neural Transm 2011; 118:713-19