Functional MRI connectivity of the primary motor cortex in functional dystonia patients.
Dystonia
Functional magnetic resonance imaging (fMRI)
Pathophysiology
Psychogenic movement disorders (PMD)
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
received:
19
07
2021
accepted:
26
10
2021
revised:
25
10
2021
pubmed:
14
11
2021
medline:
24
5
2022
entrez:
13
11
2021
Statut:
ppublish
Résumé
Functional movement disorders include a wide spectrum of clinically documented movement disorders without an apparent organic substrate. To explore the functional connectivity (FC) of the primary motor (M1) cortex in functional dystonia (FD) patients relative to healthy controls, with a focus on different clinical phenotypes. Forty FD patients (12 fixed [FixFD]; 28 mobile [MobFD]) and 43 healthy controls (14 young FixFD-age-matched [yHC]; 29 old MobFD-age-matched [oHC]) underwent resting state fMRI. A seed-based FC analysis was performed using bilateral M1 as regions of interest. Compared to controls, FD patients showed reduced FC between left M1 and left dorsal anterior cingulate cortex, and between right M1 and left M1, premotor/supplementary motor area (SMA), dorsal posterior cingulate cortex (PCC), and bilateral precuneus. Relative to yHC, FixFD patients showed reduced FC between M1 and precuneus bilaterally. Compared to oHC, MobFD patients revealed reduced FC between right M1 and left M1, premotor/SMA, dorsal-PCC, bilateral primary sensory cortices and parieto-occipital areas, and increased FC of right M1 with right associative visual cortex and bilateral ventral-PCC. FixFD patients, relative to MobFD, showed lower FC between the right M1 and right associative visual area, and bilateral precuneus and ventral-PCC. This study suggests an altered brain FC of the motor circuit with areas involved in emotional processes and sense of agency in FD. FixFD patients showed FC abnormalities mainly in areas related to sense of agency, while MobFD in regions involved in sensorimotor functions (reduced FC) and emotional processing (increased FC).
Sections du résumé
BACKGROUND
BACKGROUND
Functional movement disorders include a wide spectrum of clinically documented movement disorders without an apparent organic substrate.
OBJECTIVE
OBJECTIVE
To explore the functional connectivity (FC) of the primary motor (M1) cortex in functional dystonia (FD) patients relative to healthy controls, with a focus on different clinical phenotypes.
METHODS
METHODS
Forty FD patients (12 fixed [FixFD]; 28 mobile [MobFD]) and 43 healthy controls (14 young FixFD-age-matched [yHC]; 29 old MobFD-age-matched [oHC]) underwent resting state fMRI. A seed-based FC analysis was performed using bilateral M1 as regions of interest.
RESULTS
RESULTS
Compared to controls, FD patients showed reduced FC between left M1 and left dorsal anterior cingulate cortex, and between right M1 and left M1, premotor/supplementary motor area (SMA), dorsal posterior cingulate cortex (PCC), and bilateral precuneus. Relative to yHC, FixFD patients showed reduced FC between M1 and precuneus bilaterally. Compared to oHC, MobFD patients revealed reduced FC between right M1 and left M1, premotor/SMA, dorsal-PCC, bilateral primary sensory cortices and parieto-occipital areas, and increased FC of right M1 with right associative visual cortex and bilateral ventral-PCC. FixFD patients, relative to MobFD, showed lower FC between the right M1 and right associative visual area, and bilateral precuneus and ventral-PCC.
CONCLUSIONS
CONCLUSIONS
This study suggests an altered brain FC of the motor circuit with areas involved in emotional processes and sense of agency in FD. FixFD patients showed FC abnormalities mainly in areas related to sense of agency, while MobFD in regions involved in sensorimotor functions (reduced FC) and emotional processing (increased FC).
Identifiants
pubmed: 34773159
doi: 10.1007/s00415-021-10879-x
pii: 10.1007/s00415-021-10879-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2961-2971Subventions
Organisme : ministarstvo prosvete, nauke i tehnološkog razvoja
ID : #175090
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany.
Références
Albanese A, Bhatia K, Bressman SB, Delong MR, Fahn S, Fung VS, Hallett M, Jankovic J, Jinnah HA, Klein C, Lang AE, Mink JW, Teller JK (2013) Phenomenology and classification of dystonia: a consensus update. Mov Disord 28:863–873
pubmed: 23649720
pmcid: 3729880
doi: 10.1002/mds.25475
Apps MA, Rushworth MF, Chang SW (2016) The anterior cingulate gyrus and social cognition: tracking the motivation of others. Neuron 90:692–707
pubmed: 27196973
pmcid: 4885021
doi: 10.1016/j.neuron.2016.04.018
Aybek S, Vuilleumier P (2016) Imaging studies of functional neurologic disorders. Handb Clin Neurol 139:73–84
pubmed: 27719879
doi: 10.1016/B978-0-12-801772-2.00007-2
Baizabal-Carvallo JF, Hallett M, Jankovic J (2019) Pathogenesis and pathophysiology of functional (psychogenic) movement disorders. Neurobiol Dis 127:32–44
pubmed: 30798005
doi: 10.1016/j.nbd.2019.02.013
Barbey A, Aybek S (2017) Functional movement disorders. Curr Opin Neurol 30:427–434
pubmed: 28590986
doi: 10.1097/WCO.0000000000000464
Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos T R Soc B 360:1001–1013
doi: 10.1098/rstb.2005.1634
Blakemore RL, Sinanaj I, Galli S, Aybek S, Vuilleumier P (2016) Aversive stimuli exacerbate defensive motor behaviour in motor conversion disorder. Neuropsychologia 93:229–241
pubmed: 27842291
doi: 10.1016/j.neuropsychologia.2016.11.005
Burgmer M, Konrad C, Jansen A, Kugel H, Sommer J, Heindel W, Ringelstein EB, Heuft G, Knecht S (2006) Abnormal brain activation during movement observation in patients with conversion paralysis. Neuroimage 29:1336–1343
pubmed: 16213162
doi: 10.1016/j.neuroimage.2005.08.033
Burke RE, Fahn S, Marsden CD, Bressman SB, Moskowitz C, Friedman J (1985) Validity and reliability of a rating scale for the primary torsion dystonias. Neurology 35:73–77
pubmed: 3966004
doi: 10.1212/WNL.35.1.73
Canu E, Agosta F, Tomic A, Sarasso E, Petrovic I, Piramide N, Svetel M, Inuggi A, Miskovic ND, Kostic VS, Filippi M (2020) Breakdown of the affective-cognitive network in functional dystonia. Human Brain Mapp 41:3059–3076 https://doi.org/10.1002/hbm.24997
doi: 10.1002/hbm.24997
Carlson EB, Putnam FW, Ross CA, Torem M, Coons P, Dill DL, Loewenstein RJ, Braun BG (1993) Validity of the Dissociative Experiences Scale in screening for multiple personality disorder: a multicenter study. Am J Psychiatry 150:1030–1036
pubmed: 8317572
doi: 10.1176/ajp.150.7.1030
Cojan Y, Waber L, Schwartz S, Rossier L, Forster A, Vuilleumier P (2009) The brain under self-control: modulation of inhibitory and monitoring cortical networks during hypnotic paralysis. Neuron 62:862–875
pubmed: 19555654
doi: 10.1016/j.neuron.2009.05.021
Comella CL, Leurgans S, Wuu J, Stebbins GT, Chmura T, Dystonia Study G (2003) Rating scales for dystonia: a multicenter assessment. Mov Disord 18:303–312
pubmed: 12621634
doi: 10.1002/mds.10377
Espay AJ, Aybek S, Carson A, Edwards MJ, Goldstein LH, Hallett M, LaFaver K, LaFrance WC Jr, Lang AE, Nicholson T, Nielsen G, Reuber M, Voon V, Stone J, Morgante F (2018) Current concepts in diagnosis and treatment of functional neurological disorders. JAMA Neurol 75:1132–1141
pubmed: 29868890
pmcid: 7293766
doi: 10.1001/jamaneurol.2018.1264
Espay AJ, Lang AE (2015) Phenotype-specific diagnosis of functional (psychogenic) movement disorders. Curr Neurol Neurosci Rep 15:32
pubmed: 25900093
doi: 10.1007/s11910-015-0556-y
Espay AJ, Maloney T, Vannest J, Norris MM, Eliassen JC, Neefus E, Allendorfer JB, Chen R, Szaflarski JP (2018) Dysfunction in emotion processing underlies functional (psychogenic) dystonia. Mov Disord 33:136–145
pubmed: 29124784
doi: 10.1002/mds.27217
Espay AJ, Maloney T, Vannest J, Norris MM, Eliassen JC, Neefus E, Allendorfer JB, Lang AE, Szaflarski JP (2018) Impaired emotion processing in functional (psychogenic) tremor: a functional magnetic resonance imaging study. NeuroImage Clin 17:179–187
pubmed: 29085776
doi: 10.1016/j.nicl.2017.10.020
Fahn S, Williams DT (1988) Psychogenic dystonia. Adv Neurol 50:431–455
pubmed: 3400501
Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198
pubmed: 1202204
doi: 10.1016/0022-3956(75)90026-6
Galli S, Bereau M, Magnin E, Moulin T, Aybek S (2020) Functional movement disorders. Revue Neurologique 176:244–251
pubmed: 31606137
doi: 10.1016/j.neurol.2019.08.007
Gupta A, Lang AE (2009) Psychogenic movement disorders. Curr Opin Neurol 22:430–436
pubmed: 19542886
doi: 10.1097/WCO.0b013e32832dc169
Hallett M (2016) Functional (psychogenic) movement disorders - Clinical presentations. Parkinsonism Relat Disord 22(Suppl 1):S149-152
pubmed: 26365778
doi: 10.1016/j.parkreldis.2015.08.036
Hamilton M (1959) The assessment of anxiety states by rating. Br J Med Psychol 32:50–55
pubmed: 13638508
doi: 10.1111/j.2044-8341.1959.tb00467.x
Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62
pubmed: 14399272
pmcid: 495331
doi: 10.1136/jnnp.23.1.56
Hedera P (2012) Metabolic hyperactivity of the medial posterior parietal lobes in psychogenic tremor. Tremor Other Hyperkinetic Mov 2:02
doi: 10.5334/tohm.102
Heilbronner SR, Hayden BY (2016) Dorsal anterior cingulate cortex: a bottom-up view. Annu Rev Neurosci 39:149–170
pubmed: 27090954
pmcid: 5512175
doi: 10.1146/annurev-neuro-070815-013952
Hinson VK, Cubo E, Comella CL, Goetz CG, Leurgans S (2005) Rating scale for psychogenic movement disorders: scale development and clinimetric testing. Move Disord 20:1592–1597
doi: 10.1002/mds.20650
Kostic VS, Agosta F, Tomic A, Sarasso E, Kresojevic N, Basaia S, Svetel M, Copetti M, Filippi M (2021) Brain structural alterations in patients with GCH1 mutations associated DOPA-responsive dystonia. J Neurol Neurosurg Psychiatry 92:332–333
pubmed: 33087420
doi: 10.1136/jnnp-2020-324535
LaFaver K, Lang AE, Stone J, Morgante F, Edwards M, Lidstone S, Maurer CW, Hallett M, Dwivedi AK, Espay AJ (2020) Opinions and clinical practices related to diagnosing and managing functional (psychogenic) movement disorders: changes in the last decade. Eur J Neurol 27:975–984
pubmed: 32153070
doi: 10.1111/ene.14200
Leech R, Sharp DJ (2014) The role of the posterior cingulate cortex in cognition and disease. Brain 137:12–32
pubmed: 23869106
doi: 10.1093/brain/awt162
Maguire F, Reilly RB, Simonyan K (2020) Normal temporal discrimination in musician’s dystonia is linked to aberrant sensorimotor processing. Mov Disord 35:800–807
pubmed: 31930574
pmcid: 7818836
doi: 10.1002/mds.27984
Marin RS, Biedrzycki RC, Firinciogullari S (1991) Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res 38:143–162
pubmed: 1754629
doi: 10.1016/0165-1781(91)90040-V
Maurer CW, LaFaver K, Ameli R, Epstein SA, Hallett M, Horovitz SG (2016) Impaired self-agency in functional movement disorders: a resting-state fMRI study. Neurology 87:564–570
pubmed: 27385746
pmcid: 4977370
Maurer CW, LaFaver K, Limachia GS, Capitan G, Ameli R, Sinclair S, Epstein SA, Hallett M, Horovitz SG (2018) Gray matter differences in patients with functional movement disorders. Neurology 91:e1870–e1879
pubmed: 30305450
pmcid: 6260194
doi: 10.1212/WNL.0000000000006514
Nijenhuis ER, Spinhoven P, Van Dyck R, Van der Hart O, Vanderlinden J (1996) The development and psychometric characteristics of the Somatoform Dissociation Questionnaire (SDQ-20). J Nerv Ment Dis 184:688–694
pubmed: 8955682
doi: 10.1097/00005053-199611000-00006
Petrovic IN, Tomic A, Voncina MM, Pesic D, Kostic VS (2018) Characteristics of two distinct clinical phenotypes of functional (psychogenic) dystonia: follow-up study. J Neurol 265:82–88
pubmed: 29143206
doi: 10.1007/s00415-017-8667-9
Roelofs JJ, Teodoro T, Edwards MJ (2019) Neuroimaging in Functional Movement Disorders. Curr Neurol Neurosci Rep 19:12
pubmed: 30747347
pmcid: 6373326
doi: 10.1007/s11910-019-0926-y
Rolls ET (2019) The cingulate cortex and limbic systems for emotion, action, and memory. Brain Struct Funct 224:3001–3018
pubmed: 31451898
pmcid: 6875144
doi: 10.1007/s00429-019-01945-2
Sarasso E, Agosta F, Piramide N, Bianchi F, Butera C, Gatti R, Amadio S, Del Carro U, Filippi M (2020) Sensory trick phenomenon in cervical dystonia: a functional MRI study. J Neurol 267:1103–1115
pubmed: 31897600
doi: 10.1007/s00415-019-09683-5
Sarasso E, Agosta F, Temporiti F, Adamo P, Piccolo F, Copetti M, Gatti R, Filippi M (2018) Brain motor functional changes after somatosensory discrimination training. Brain Imaging Behav 12:1011–1021
pubmed: 28861843
doi: 10.1007/s11682-017-9763-2
Schmerler DA, Espay AJ (2016) Functional dystonia. Handb Clin Neurol 139:235–245
pubmed: 27719842
doi: 10.1016/B978-0-12-801772-2.00020-5
Schrag AE, Mehta AR, Bhatia KP, Brown RJ, Frackowiak RS, Trimble MR, Ward NS, Rowe JB (2013) The functional neuroimaging correlates of psychogenic versus organic dystonia. Brain 136:770–781
pubmed: 23436503
pmcid: 3580272
doi: 10.1093/brain/awt008
Tomic A, Agosta F, Sarasso E, Petrovic I, Basaia S, Pesic D, Kostic M, Fontana A, Kostic VS, Filippi M (2018) Are there two different forms of functional dystonia? A multimodal brain structural MRI study. Mol Psychiatry 25:3350–3359
pubmed: 30120414
doi: 10.1038/s41380-018-0222-2
Tomic A, Agosta F, Sarasso E, Svetel M, Kresojevic N, Fontana A, Canu E, Petrovic I, Kostic VS, Filippi M (2021) Brain structural changes in focal dystonia-what about task specificity? A multimodal MRI study. Mov Disord 36:196–205
pubmed: 32979238
doi: 10.1002/mds.28304
van Beilen M, de Jong BM, Gieteling EW, Renken R, Leenders KL (2011) Abnormal parietal function in conversion paresis. PLoS ONE 6:e25918
pubmed: 22039428
pmcid: 3200327
doi: 10.1371/journal.pone.0025918
Vogt BA (2016) Midcingulate cortex: Structure, connections, homologies, functions and diseases. J Chem Neuroanat 74:28–46
pubmed: 26993424
doi: 10.1016/j.jchemneu.2016.01.010
Vogt BA, Vogt L, Laureys S (2006) Cytology and functionally correlated circuits of human posterior cingulate areas. Neuroimage 29:452–466
pubmed: 16140550
doi: 10.1016/j.neuroimage.2005.07.048
Voon V, Brezing C, Gallea C, Hallett M (2011) Aberrant supplementary motor complex and limbic activity during motor preparation in motor conversion disorder. Mov Disord 26:2396–2403
pubmed: 21935985
pmcid: 4162742
doi: 10.1002/mds.23890
Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC (1996) A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4:58–73
pubmed: 20408186
doi: 10.1002/(SICI)1097-0193(1996)4:1<58::AID-HBM4>3.0.CO;2-O