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 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Journal of Neurology
Published in: Journal of Neurology 3/2018

01-03-2018 | Original Communication

Distinct manifestation of cognitive deficits associate with different resting-state network disruptions in non-demented patients with Parkinson’s disease

Authors: Kazuya Kawabata, Hirohisa Watanabe, Kazuhiro Hara, Epifanio Bagarinao, Noritaka Yoneyama, Aya Ogura, Kazunori Imai, Michihito Masuda, Takamasa Yokoi, Reiko Ohdake, Yasuhiro Tanaka, Takashi Tsuboi, Tomohiko Nakamura, Masaaki Hirayama, Mizuki Ito, Naoki Atsuta, Satoshi Maesawa, Shinji Naganawa, Masahisa Katsuno, Gen Sobue

Published in: Journal of Neurology | Issue 3/2018

Login to get access

Abstract

Cognitive deficits in Parkinson’s disease (PD) are heterogeneous entities, but a relationship between the heterogeneity of cognitive deficits and resting-state network (RSN) changes remains elusive. In this study, we examined five sub-domain scores according to Addenbrooke’s Cognitive Examination-Revised (ACE-R) for the cognitive evaluation and classification of 72 non-demented patients with PD. Twenty-eight patients were classified as PD with normal cognition (PD-NC). The remaining 44 were subdivided into the following 2 groups using a hierarchical cluster analysis: 20 with a predominant decrease in memory (PD with amnestic cognitive deficits: PD-A) and 24 with good memory who exhibited a decrease in other sub-domains (PD with non-amnestic cognitive deficits: PD-NA). We used an independent component analysis of RS-fMRI data to investigate the inter-group differences of RSN. Compared to the controls, the PD-A showed lower FC within the ventral default mode network (vDMN) and the visuospatial network. On the other hand, the PD-NA showed lower FC within the visual networks and the cerebellum–brainstem network. Significant differences in the FC within the vDMN and cerebellum–brainstem network were observed between the PD-A and PD-NA, which provided a good discrimination between PD-A and PD-NA using a support vector machine. Distinct patterns of cognitive deficits correspond to different RSN changes.
Appendix
Available only for authorised users
Literature
1.
Aarsland D, Perry R, Brown A, Larsen JP, Ballard C (2005) Neuropathology of dementia in Parkinson’s disease: a prospective, community-based study. Ann Neurol 58:773–776CrossRefPubMed
2.
Abe Y, Kachi T, Kato T, Arahata Y, Yamada T, Washimi Y, Iwai K, Ito K, Yanagisawa N, Sobue G (2003) Occipital hypoperfusion in Parkinson’s disease without dementia: correlation to impaired cortical visual processing. J Neurol Neurosurg Psychiatry 74:419–422CrossRefPubMedPubMedCentral
3.
Agosta F, Canu E, Stefanova E, Sarro L, Tomic A, Spica V, Comi G, Kostic VS, Filippi M (2014) Mild cognitive impairment in Parkinson’s disease is associated with a distributed pattern of brain white matter damage. Hum Brain Mapp 35:1921–1929CrossRefPubMed
4.
Agosta F, Kostic VS, Davidovic K, Kresojevic N, Sarro L, Svetel M, Stankovic I, Comi G, Klein C, Filippi M (2013) White matter abnormalities in Parkinson’s disease patients with glucocerebrosidase gene mutations. Mov Disord 28:772–778CrossRefPubMed
5.
6.
Baciu M, Boudiaf N, Cousin E, Perrone-Bertolotti M, Pichat C, Fournet N, Chainay H, Lamalle L, Krainik A (2016) Functional MRI evidence for the decline of word retrieval and generation during normal aging. Age (Dordr) 38:3CrossRef
7.
Baggio HC, Sala-Llonch R, Segura B, Marti MJ, Valldeoriola F, Compta Y, Tolosa E, Junque C (2014) Functional brain networks and cognitive deficits in Parkinson’s disease. Hum Brain Mapp 35:4620–4634CrossRefPubMed
8.
Baggio HC, Segura B, Sala-Llonch R, Marti MJ, Valldeoriola F, Compta Y, Tolosa E, Junque C (2015) Cognitive impairment and resting-state network connectivity in Parkinson’s disease. Hum Brain Mapp 36:199–212CrossRefPubMed
9.
Barkhof F, Haller S, Rombouts SA (2014) Resting-state functional MR imaging: a new window to the brain. Radiology 272:29–49CrossRefPubMed
10.
Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360:1001–1013CrossRefPubMedPubMedCentral
11.
Berankova D, Janousova E, Mrackova M, Eliasova I, Kostalova M, Skutilova S, Rektorova I (2015) Addenbrooke’s cognitive examination and individual domain cut-off scores for discriminating between different cognitive subtypes of parkinson’s disease. Parkinsons Dis 2015:579417PubMedPubMedCentral
12.
Birn RM, Kenworthy L, Case L, Caravella R, Jones TB, Bandettini PA, Martin A (2010) Neural systems supporting lexical search guided by letter and semantic category cues: a self-paced overt response fMRI study of verbal fluency. Neuroimage 49:1099–1107CrossRefPubMed
13.
Bohnen NI, Koeppe RA, Minoshima S, Giordani B, Albin RL, Frey KA, Kuhl DE (2011) Cerebral glucose metabolic features of Parkinson disease and incident dementia: longitudinal study. J Nucl Med 52:848–855CrossRefPubMed
14.
Bohnen NI, Minoshima S, Giordani B, Frey KA, Kuhl DE (1999) Motor correlates of occipital glucose hypometabolism in Parkinson’s disease without dementia. Neurology 52:541–546CrossRefPubMed
15.
Caillava-Santos F, Margis R, de Mello Rieder CR (2015) Wearing-off in Parkinson’s disease: neuropsychological differences between on and off periods. Neuropsychiatr Dis Treat 11:1175–1180CrossRefPubMedPubMedCentral
16.
Chang C-C (2011) LIBSVM: a library for support vector machines. ACM Trans Intell Syst Technol 2:3–27CrossRef
17.
Cholerton BA, Zabetian CP, Wan JY, Montine TJ, Quinn JF, Mata IF, Chung KA, Peterson A, Espay AJ, Revilla FJ, Devoto J, Watson GS, Hu SC, Leverenz JB, Edwards KL (2014) Evaluation of mild cognitive impairment subtypes in Parkinson’s disease. Mov Disord 29:756–764CrossRefPubMedPubMedCentral
18.
Cortes C, Vapnik V (1995) Support-vector networks. Mach Learn 20:273–297
19.
Cortese A, Amano K, Koizumi A, Lau H, Kawato M (2017) Decoded fMRI neurofeedback can induce bidirectional confidence changes within single participants. Neuroimage 149:323–337CrossRefPubMedPubMedCentral
20.
Delgado-Alvarado M, Gago B, Navalpotro-Gomez I, Jimenez-Urbieta H, Rodriguez-Oroz MC (2016) Biomarkers for dementia and mild cognitive impairment in Parkinson’s disease. Mov Disord 31:861–881CrossRefPubMed
21.
Dos Santos Kawata KH, Hashimoto R, Nishio Y, Hayashi A, Ogawa N, Kanno S, Hiraoka K, Yokoi K, Iizuka O, Mori E (2012) A validation study of the Japanese version of the Addenbrooke’s cognitive examination-revised. Dement Geriatr Cogn Dis Extra 2:29–37CrossRefPubMedPubMedCentral
22.
Dubois B, Burn D, Goetz C, Aarsland D, Brown RG, Broe GA, Dickson D, Duyckaerts C, Cummings J, Gauthier S, Korczyn A, Lees A, Levy R, Litvan I, Mizuno Y, McKeith IG, Olanow CW, Poewe W, Sampaio C, Tolosa E, Emre M (2007) Diagnostic procedures for Parkinson’s disease dementia: recommendations from the movement disorder society task force. Mov Disord 22:2314–2324CrossRefPubMed
23.
Eberling JL, Richardson BC, Reed BR, Wolfe N, Jagust WJ (1994) Cortical glucose metabolism in Parkinson’s disease without dementia. Neurobiol Aging 15:329–335CrossRefPubMed
24.
Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335CrossRefPubMed
25.
26.
Esposito F, Tessitore A, Giordano A, De Micco R, Paccone A, Conforti R, Pignataro G, Annunziato L, Tedeschi G (2013) Rhythm-specific modulation of the sensorimotor network in drug-naive patients with Parkinson’s disease by levodopa. Brain 136:710–725CrossRefPubMed
27.
Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol 149:351–356CrossRefPubMed
28.
Filippini N, MacIntosh BJ, Hough MG, Goodwin GM, Frisoni GB, Smith SM, Matthews PM, Beckmann CF, Mackay CE (2009) Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci USA 106:7209–7214CrossRefPubMedPubMedCentral
29.
30.
Gottlich M, Munte TF, Heldmann M, Kasten M, Hagenah J, Kramer UM (2013) Altered resting state brain networks in Parkinson’s disease. PLoS ONE 8:e77336CrossRefPubMedPubMedCentral
31.
Harrington DL, Shen Q, Castillo GN, Filoteo JV, Litvan I, Takahashi C, French C (2017) Aberrant intrinsic activity and connectivity in cognitively normal Parkinson’s disease. Front Aging Neurosci 9:197CrossRefPubMedPubMedCentral
32.
Hendershott TR, Zhu D, Llanes S, Poston KL (2017) Domain-specific accuracy of the montreal cognitive assessment subsections in Parkinson’s disease. Parkinsonism Relat Disord 38:31–34CrossRefPubMed
33.
Hughes AJ, Ben-Shlomo Y, Daniel SE, Lees AJ (1992) What features improve the accuracy of clinical diagnosis in Parkinson’s disease: a clinicopathologic study. Neurology 42:1142–1146CrossRefPubMed
34.
Irwin DJ, Grossman M, Weintraub D, Hurtig HI, Duda JE, Xie SX, Lee EB, Van Deerlin VM, Lopez OL, Kofler JK, Nelson PT, Jicha GA, Woltjer R, Quinn JF, Kaye J, Leverenz JB, Tsuang D, Longfellow K, Yearout D, Kukull W, Keene CD, Montine TJ, Zabetian CP, Trojanowski JQ (2017) Neuropathological and genetic correlates of survival and dementia onset in synucleinopathies: a retrospective analysis. Lancet Neurol 16:55–65CrossRefPubMedPubMedCentral
35.
36.
Kalaitzakis ME, Christian LM, Moran LB, Graeber MB, Pearce RK, Gentleman SM (2009) Dementia and visual hallucinations associated with limbic pathology in Parkinson’s disease. Parkinsonism Relat Disord 15:196–204CrossRefPubMed
37.
Kansal K, Yang Z, Fishman AM, Sair HI, Ying SH, Jedynak BM, Prince JL, Onyike CU (2017) Structural cerebellar correlates of cognitive and motor dysfunctions in cerebellar degeneration. Brain 140:707–720PubMed
38.
Kashihara K, Kondo T, Mizuno Y, Kikuchi S, Kuno S, Hasegawa K, Hattori N, Mochizuki H, Mori H, Murata M, Nomoto M, Takahashi R, Takeda A, Tsuboi Y, Ugawa Y, Yamanmoto M, Yokochi F, Yoshii F, Stebbins GT, Tilley BC, Luo S, Wang L, LaPelle NR, Goetz CG, Group M-UJVS (2014) Official Japanese Version of the Movement Disorder Society-Unified Parkinson’s Disease Rating Scale: validation against the original English version. Mov Disord Clin Pract 1:200–212CrossRefPubMedPubMedCentral
39.
Kehagia AA, Barker RA, Robbins TW (2010) Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease. Lancet Neurol 9:1200–1213CrossRefPubMed
40.
Krajcovicova L, Mikl M, Marecek R, Rektorova I (2012) The default mode network integrity in patients with Parkinson’s disease is levodopa equivalent dose-dependent. J Neural Transm (Vienna) 119:443–454CrossRef
41.
Laird AR, Fox PM, Eickhoff SB, Turner JA, Ray KL, McKay DR, Glahn DC, Beckmann CF, Smith SM, Fox PT (2011) Behavioral interpretations of intrinsic connectivity networks. J Cogn Neurosci 23:4022–4037CrossRefPubMedPubMedCentral
42.
Lin CH, Wu RM (2015) Biomarkers of cognitive decline in Parkinson’s disease. Parkinsonism Relat Disord 21:431–443CrossRefPubMed
43.
Litvan I, Goldman JG, Troster AI, Schmand BA, Weintraub D, Petersen RC, Mollenhauer B, Adler CH, Marder K, Williams-Gray CH, Aarsland D, Kulisevsky J, Rodriguez-Oroz MC, Burn DJ, Barker RA, Emre M (2012) Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: Movement Disorder Society Task Force guidelines. Mov Disord 27:349–356CrossRefPubMedPubMedCentral
44.
McColgan P, Evans JR, Breen DP, Mason SL, Barker RA, Williams-Gray CH (2012) Addenbrooke’s Cognitive Examination-Revised for mild cognitive impairment in Parkinson’s disease. Mov Disord 27:1173–1177CrossRefPubMed
45.
Mioshi E, Dawson K, Mitchell J, Arnold R, Hodges JR (2006) The Addenbrooke’s Cognitive Examination Revised (ACE-R): a brief cognitive test battery for dementia screening. Int J Geriatr Psychiatry 21:1078–1085CrossRefPubMed
46.
Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699CrossRefPubMed
47.
Ng B, Varoquaux G, Poline JB, Thirion B, Greicius MD, Poston KL (2017) Distinct alterations in Parkinson’s medication-state and disease-state connectivity. Neuroimage Clin 16:575–585CrossRefPubMedPubMedCentral
48.
Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25CrossRefPubMed
49.
Olde Dubbelink KT, Schoonheim MM, Deijen JB, Twisk JW, Barkhof F, Berendse HW (2014) Functional connectivity and cognitive decline over 3 years in Parkinson disease. Neurology 83:2046–2053CrossRefPubMed
50.
Pedersen KF, Larsen JP, Tysnes OB, Alves G (2017) Natural course of mild cognitive impairment in Parkinson disease: a 5-year population-based study. Neurology 88:767–774CrossRefPubMed
51.
Peraza LR, Nesbitt D, Lawson RA, Duncan GW, Yarnall AJ, Khoo TK, Kaiser M, Firbank MJ, O’Brien JT, Barker RA, Brooks DJ, Burn DJ, Taylor JP (2017) Intra- and inter-network functional alterations in Parkinson’s disease with mild cognitive impairment. Hum Brain Mapp 38:1702–1715CrossRefPubMed
52.
Petersen RC, Morris JC (2005) Mild cognitive impairment as a clinical entity and treatment target. Arch Neurol 62:1160–1163 (discussion 1167) CrossRefPubMed
53.
Petrou M, Dwamena BA, Foerster BR, MacEachern MP, Bohnen NI, Muller ML, Albin RL, Frey KA (2015) Amyloid deposition in Parkinson’s disease and cognitive impairment: a systematic review. Mov Disord 30:928–935CrossRefPubMedPubMedCentral
54.
Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154CrossRefPubMed
55.
Reginold W, Duff-Canning S, Meaney C, Armstrong MJ, Fox S, Rothberg B, Zadikoff C, Kennedy N, Gill D, Eslinger P, Marshall F, Mapstone M, Chou KL, Persad C, Litvan I, Mast B, Tang-Wai D, Lang AE, Marras C (2013) Impact of mild cognitive impairment on health-related quality of life in Parkinson’s disease. Dement Geriatr Cogn Disord 36:67–75CrossRefPubMed
56.
Rittman T, Ghosh BC, McColgan P, Breen DP, Evans J, Williams-Gray CH, Barker RA, Rowe JB (2013) The Addenbrooke’s Cognitive Examination for the differential diagnosis and longitudinal assessment of patients with parkinsonian disorders. J Neurol Neurosurg Psychiatry 84:544–551CrossRefPubMedPubMedCentral
57.
Robbins TW, Cools R (2014) Cognitive deficits in Parkinson’s disease: a cognitive neuroscience perspective. Mov Disord 29:597–607CrossRefPubMed
58.
Scharnowski F, Veit R, Zopf R, Studer P, Bock S, Diedrichsen J, Goebel R, Mathiak K, Birbaumer N, Weiskopf N (2015) Manipulating motor performance and memory through real-time fMRI neurofeedback. Biol Psychol 108:85–97CrossRefPubMedPubMedCentral
59.
Shirer WR, Ryali S, Rykhlevskaia E, Menon V, Greicius MD (2012) Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex 22:158–165CrossRefPubMed
60.
Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci USA 106:13040–13045CrossRefPubMedPubMedCentral
61.
Stoodley CJ, Valera EM, Schmahmann JD (2012) Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study. Neuroimage 59:1560–1570CrossRefPubMed
62.
Szewczyk-Krolikowski K, Menke RA, Rolinski M, Duff E, Salimi-Khorshidi G, Filippini N, Zamboni G, Hu MT, Mackay CE (2014) Functional connectivity in the basal ganglia network differentiates PD patients from controls. Neurology 83:208–214CrossRefPubMedPubMedCentral
63.
Tahmasian M, Bettray LM, van Eimeren T, Drzezga A, Timmermann L, Eickhoff CR, Eickhoff SB, Eggers C (2015) A systematic review on the applications of resting-state fMRI in Parkinson’s disease: does dopamine replacement therapy play a role? Cortex 73:80–105CrossRefPubMed
64.
Tessitore A, Esposito F, Vitale C, Santangelo G, Amboni M, Russo A, Corbo D, Cirillo G, Barone P, Tedeschi G (2012) Default-mode network connectivity in cognitively unimpaired patients with Parkinson disease. Neurology 79:2226–2232CrossRefPubMed
65.
66.
Wei Q, Chen X, Zheng Z, Huang R, Guo X, Cao B, Bak TH, Shang H (2015) Screening for cognitive impairment in a Chinese ALS population. Amyotroph Lateral Scler Frontotemporal Degener 16:40–45CrossRefPubMed
67.
68.
Winblad B, Palmer K, Kivipelto M, Jelic V, Fratiglioni L, Wahlund LO, Nordberg A, Backman L, Albert M, Almkvist O, Arai H, Basun H, Blennow K, de Leon M, DeCarli C, Erkinjuntti T, Giacobini E, Graff C, Hardy J, Jack C, Jorm A, Ritchie K, van Duijn C, Visser P, Petersen RC (2004) Mild cognitive impairment–beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Intern Med 256:240–246CrossRefPubMed
69.
70.
Yahata N, Morimoto J, Hashimoto R, Lisi G, Shibata K, Kawakubo Y, Kuwabara H, Kuroda M, Yamada T, Megumi F, Imamizu H, Nanez JE Sr, Takahashi H, Okamoto Y, Kasai K, Kato N, Sasaki Y, Watanabe T, Kawato M (2016) A small number of abnormal brain connections predicts adult autism spectrum disorder. Nat Commun 7:11254CrossRefPubMedPubMedCentral
Metadata
Title
Distinct manifestation of cognitive deficits associate with different resting-state network disruptions in non-demented patients with Parkinson’s disease
Authors
Kazuya Kawabata
Hirohisa Watanabe
Kazuhiro Hara
Epifanio Bagarinao
Noritaka Yoneyama
Aya Ogura
Kazunori Imai
Michihito Masuda
Takamasa Yokoi
Reiko Ohdake
Yasuhiro Tanaka
Takashi Tsuboi
Tomohiko Nakamura
Masaaki Hirayama
Mizuki Ito
Naoki Atsuta
Satoshi Maesawa
Shinji Naganawa
Masahisa Katsuno
Gen Sobue
Publication date
01-03-2018
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 3/2018
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-018-8755-5

Other articles of this Issue 3/2018

Journal of Neurology 3/2018 Go to the issue

Original Communication

Variability of presynaptic nigrostriatal dopaminergic function and clinical heterogeneity in a dopa-responsive dystonia family with GCH-1 gene mutation

Original Communication

Impact of D-dimer levels for short-term or long-term outcomes in cryptogenic stroke patients

Short Commentary

A common CHRNE mutation in Brazilian patients with congenital myasthenic syndrome

Original Communication

CSF neurofilament proteins as diagnostic and prognostic biomarkers for amyotrophic lateral sclerosis

Original Communication

Electrophysiological and behavioral effects of frontal transcranial direct current stimulation on cognitive fatigue in multiple sclerosis

Original Communication

Glioblastoma as differential diagnosis of autoimmune encephalitis