The motor inhibitory network in patients with asymmetrical Parkinson's disease: An fMRI study.
Dopamine
Functional connectivity
Imaging
Inhibition
Parkinson’s disease
Stop-signal reaction time task
Subthalamic nucleus
fMRI
Journal
Brain imaging and behavior
ISSN: 1931-7565
Titre abrégé: Brain Imaging Behav
Pays: United States
ID NLM: 101300405
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
accepted:
13
10
2021
pubmed:
13
1
2022
medline:
18
5
2022
entrez:
12
1
2022
Statut:
ppublish
Résumé
Recent imaging studies with the stop-signal task in healthy individuals indicate that the subthalamic nucleus, the pre-supplementary motor area and the inferior frontal gyrus are key components of the right hemisphere "inhibitory network". Limited information is available regarding neural substrates of inhibitory processing in patients with asymmetric Parkinson's disease. The aim of the current fMRI study was to identify the neural changes underlying deficient inhibitory processing on the stop-signal task in patients with predominantly left-sided Parkinson's disease. Fourteen patients and 23 healthy controls performed a stop-signal task with the left and right hands. Behaviorally, patients showed delayed response inhibition with either hand compared to controls. We found small imaging differences for the right hand, however for the more affected left hand when behavior was successfully inhibited we found reduced activation of the inferior frontal gyrus bilaterally and the insula. Using the stop-signal delay as regressor, contralateral underactivation in the right dorsolateral prefrontal cortex, inferior frontal and anterior putamen were found in patients. This finding indicates dysfunction of the right inhibitory network in left-sided Parkinson's disease. Functional connectivity analysis of the left subthalamic nucleus showed a significant increase of connectivity with bilateral insula. In contrast, the right subthalamic nucleus showed increased connectivity with visuomotor and sensorimotor regions of the cerebellum. We conclude that altered inhibitory control in left-sided Parkinson's disease is associated with reduced activation in regions dedicated to inhibition in healthy controls, which requires engagement of additional regions, not observed in controls, to successfully stop ongoing actions.
Identifiants
pubmed: 35020124
doi: 10.1007/s11682-021-00587-5
pii: 10.1007/s11682-021-00587-5
pmc: PMC9107438
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1349-1361Subventions
Organisme : Centro de Investigación Médica Aplicada, Universidad de Navarra
ID : 2018.071
Informations de copyright
© 2022. The Author(s).
Références
Arimura N, Nakayama Y, Yamagata T, Tanji J, Hoshi E (2013). Involvement of the globus pallidus in behavioral goal determination and action specification. J Neurosci, 33(34), 13639–13653.
Aron, A. R. (2011). From reactive to proactive and selective control: Developing a richer model for stopping inappropriate responses. Biological Psychiatry, 69, e55-68.
pubmed: 20932513
doi: 10.1016/j.biopsych.2010.07.024
Aron, A. R., Behrens, T. E., Smith, S., Frank, M. J., & Poldrack, R. A. (2007). Triangulating a Cognitive Control Network Using Diffusion-Weighted Magnetic Resonance Imaging (MRI) and Functional MRI. Journal of Neuroscience, 27(14), 3743–3752.
pubmed: 17409238
doi: 10.1523/JNEUROSCI.0519-07.2007
Aron, A. R., & Poldrack, R. A. (2006). Cortical and Subcortical Contributions to Stop Signal Response Inhibition: Role of the Subthalamic Nucleus. Journal of Neuroscience, 26, 2424–2433.
pubmed: 16510720
doi: 10.1523/JNEUROSCI.4682-05.2006
Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6, 115–116.
pubmed: 12536210
doi: 10.1038/nn1003
Ashburner, J., & Friston, K. J. (2005). Unified segmentation. NeuroImage, 26, 839–851.
pubmed: 15955494
doi: 10.1016/j.neuroimage.2005.02.018
Aumann, M., Stark, A. J., Hughes, S. B., Lin, Y.-C., Kang, H., Bradley, E., Zald, D. H., & Claassen, D. O. (2020). Self-reported rates of impulsivity in Parkinson’s Disease. Annals of Clinical and Translational Neurology, 7(4), 437–448.
pubmed: 32227451
pmcid: 7187703
doi: 10.1002/acn3.51016
Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961). An inventory for measuring depression. Arch Gen Psychiatry, 4, 561–71
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc B, 57, 289–300.
Bergman, H., Wichmann, T., & DeLong, M. R. (1990). Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science, 249(80), 1436–1438.
pubmed: 2402638
doi: 10.1126/science.2402638
Bostan AC, Dum RP, Strick PL (2010). The basal ganglia communicate with the cerebellum. Proc Natl Acad Sci, 107, 8452–8456.
Cerasa, A., Donzuso, G., Morelli, M., Mangone, G., Salsone, M., Passamonti, L., Augimeri, A., Arabia, G., & Quattrone, A. (2015). The motor inhibition system in Parkinson’s disease with levodopa-induced dyskinesias. Movement Disorders, 30, 1912–1920.
pubmed: 26275050
doi: 10.1002/mds.26378
Cogent 2000 (RRID:SCR_015672). http://www.vislab.ucl.ac.uk/cogent_2000.php
Chen, W., de Hemptinne, C., Miller, A. M., Leibbrand, M., Little, S. J., Lim, D. A., Larson, P. S., & Starr, P. A. (2020). Prefrontal-Subthalamic Hyperdirect Pathway Modulates Movement Inhibition in Humans. Neuron, 106, 579-588.e3.
pubmed: 32155442
pmcid: 7274135
doi: 10.1016/j.neuron.2020.02.012
Duann, J.-R.R., Ide, J. S., Luo, X., & Li, C. S. R. (2009). Functional connectivity delineates distinct roles of the inferior frontal cortex and presupplementary motor area in stop signal inhibition. Journal of Neuroscience, 29, 10171–10179.
pubmed: 19675251
doi: 10.1523/JNEUROSCI.1300-09.2009
Erga, H. E., Alves, G., Larsen, J. P., Tysnes, O. B., & Pedersen, K. F. (2017). Impulsive and Compulsive Behaviors in Parkinson’s Disease: The Norwegian ParkWest Study. Journal of Parkinson’s Disease, 7, 183–191.
pubmed: 27911342
pmcid: 5302042
doi: 10.3233/JPD-160977
Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.
pubmed: 1202204
doi: 10.1016/0022-3956(75)90026-6
Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997). Psychophysiological and modulatory interactions in neuroimaging. Neuroimage, 6 (3), 218–29.
Friston, K. (1994). Functional and effective connectivity in neuroimaging: A synthesis. Human Brain Mapping, 2, 56–78.
doi: 10.1002/hbm.460020107
Garavan, H., Ross, T. J., Stein, E., & a,. (1999). Right hemispheric dominance of inhibitory control: An event-related functional MRI study. Proc Natl Acad Sci U S A, 96, 8301–8306.
pubmed: 10393989
pmcid: 22229
doi: 10.1073/pnas.96.14.8301
Gauggel, S., Rieger, M., & Feghoff, T. A. (2004). Inhibition of ongoing responses in patients with Parkinson’s disease. Journal of Neurology, Neurosurgery and Psychiatry, 75, 539–544.
pubmed: 15026491
pmcid: 1739013
doi: 10.1136/jnnp.2003.016469
Genovese CR, Lazar NA, Nichols T (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage, 15(4), 870–878.
Gitelman, D. R., Penny, W. D., Ashburner, J., & Friston, K. J. (2003). Modeling regional and psychophysiologic interactions in fMRI: The importance of hemodynamic deconvolution. NeuroImage, 19, 200–207.
pubmed: 12781739
doi: 10.1016/S1053-8119(03)00058-2
Hampshire, A., Chamberlain, S. R., Monti, M. M., Duncan, J., & Owen, A. M. (2010). The role of the right inferior frontal gyrus: Inhibition and attentional control. NeuroImage, 50, 1313–1319.
pubmed: 20056157
doi: 10.1016/j.neuroimage.2009.12.109
Hoehn, M. M., & Yahr, M. D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17, 427–442.
pubmed: 6067254
doi: 10.1212/WNL.17.5.427
Hughes A J, Daniel S E, Kilford L, Lees A J. (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. Journal of Neurology Neurosurgery and Psychiatry, 55(3):181–4. https://doi.org/10.1136/jnnp.55.3.181 .
Jahanshahi, M., Jenkins, I. H., Brown, R. G., Marsden, C. D., Passingham, R. E., & Brooks, D. J. (1995). Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain, 118(Pt 4), 913–933.
pubmed: 7655888
doi: 10.1093/brain/118.4.913
Jahanshahi, M., Obeso, I., Rothwell, J. C., & Obeso, J. A. (2015). A fronto-striato-subthalamic-pallidal network for goal-directed and habitual inhibition. Nature Reviews Neuroscience, 16, 719–732.
pubmed: 26530468
doi: 10.1038/nrn4038
Jahfari, S., Waldorp, L., van den Wildenberg, W. P. M., Scholte, H. S., Ridderinkhof, K. R., & Forstmann, B. U. (2011). Effective Connectivity Reveals Important Roles for Both the Hyperdirect (Fronto-Subthalamic) and the Indirect (Fronto-Striatal-Pallidal) Fronto-Basal Ganglia Pathways during Response Inhibition. Journal of Neuroscience, 31, 6891–6899.
pubmed: 21543619
doi: 10.1523/JNEUROSCI.5253-10.2011
Kohl, S., Aggeli, K., Obeso, I., Speekenbrink, M., Limousin, P., Kuhn, J., & Jahanshahi, M. (2015). In Parkinson’s disease pallidal deep brain stimulation speeds up response initiation but has no effect on reactive inhibition. Journal of Neurology, 262, 1741–1750.
pubmed: 25963101
doi: 10.1007/s00415-015-7768-6
Li, C. S. R., Yan, P., Chao, H. H., & a, Sinha R, Paliwal P, Constable RT, Zhang S, Lee TW,. (2008). Error-specific medial cortical and subcortical activity during the stop signal task: A functional magnetic resonance imaging study. Neuroscience, 155, 1142–1151.
pubmed: 18674592
doi: 10.1016/j.neuroscience.2008.06.062
Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage, 19(3), 1233–1239.
Manza P, Schwartz G, Masson M, Kann S, Volkow ND, Li C-SR, Leung H-C (2018). Levodopa improves response inhibition and enhances striatal activation in early-stage Parkinson’s disease. Neurobiol Aging, 66, 12–22.
Milardi, D., Gaeta, M., Marino, S., Arrigo, A., Vaccarino, G., Mormina, E., Rizzo, G., Milazzo, C., Finocchio, G., Baglieri, A., Anastasi, G., & Quartarone, A. (2015). Basal ganglia network by constrained spherical deconvolution: A possible cortico-pallidal pathway? Movement Disorders, 30, 342–349.
pubmed: 25156805
doi: 10.1002/mds.25995
Mirabella, G., Fragola, M., Giannini, G., Modugno, N., & Lakens, D. (2017). Inhibitory control is not lateralized in Parkinson’s patients. Neuropsychologia, 102, 177–189.
pubmed: 28647437
doi: 10.1016/j.neuropsychologia.2017.06.025
Mosher, C. P., Mamelak, A. N., Malekmohammadi, M., Pouratian, N., & Rutishauser, U. (2021). Distinct roles of dorsal and ventral subthalamic neurons in action selection and cancellation. Neuron, 109, 869-881.e6.
pubmed: 33482087
pmcid: 7933114
doi: 10.1016/j.neuron.2020.12.025
Obeso, I., Cho, S. S., Antonelli, F., Houle, S., Jahanshahi, M., Ko, J. H., & Strafella, A. P. (2013). Stimulation of the pre-SMA influences cerebral blood flow in frontal areas involved with inhibitory control of action. Brain Stimulation, 6, 769–776.
pubmed: 23545472
doi: 10.1016/j.brs.2013.02.002
Obeso, I., Wilkinson, L., Casabona, E., Bringas, M. L., Álvarez, M., Álvarez, L., Pavón, N., Rodríguez-Oroz, M.-C.C., Macías, R., Obeso, J. A., & Jahanshahi, M. (2011a). Deficits in inhibitory control and conflict resolution on cognitive and motor tasks in Parkinson’s disease. Experimental Brain Research, 212, 371–384.
pubmed: 21643718
doi: 10.1007/s00221-011-2736-6
Obeso, I., Wilkinson, L., Casabona, E., Speekenbrink, M., Bringas, M. L., Álvarez, M., Álvarez, L., Pavón, N., Rodríguez-Oroz, M. C., Macías, R., Obeso, J. A., & Jahanshahi, M. (2014a). The subthalamic nucleus and inhibitory control: Impact of subthalamotomy in Parkinson’s disease. Brain, 137, 1470–1480.
pubmed: 24657985
doi: 10.1093/brain/awu058
Obeso, I., Wilkinson, L., Casabona, E., Speekenbrink, M., Luisa Bringas, M., Álvarez, M., Álvarez, L., Pavón, N., Rodríguez-Oroz, M. C., Macías, R., Obeso, J. A., & Jahanshahi, M. (2014b). The subthalamic nucleus and inhibitory control: Impact of subthalamotomy in Parkinson’s disease. Brain, 137, 1470–1480.
pubmed: 24657985
doi: 10.1093/brain/awu058
Obeso, I., Wilkinson, L., & Jahanshahi, M. (2011b). Levodopa medication does not influence motor inhibition or conflict resolution in a conditional stop-signal task in Parkinson’s disease. Experimental Brain Research, 213, 435–445.
pubmed: 21796541
doi: 10.1007/s00221-011-2793-x
Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(97), 113.
Olivito, G., Brunamonti, E., Clausi, S., Pani, P., Chiricozzi, F. R., Giamundo, M., Molinari, M., Leggio, M., & Ferraina, S. (2017). Atrophic degeneration of cerebellum impairs both the reactive and the proactive control of movement in the stop signal paradigm. Experimental Brain Research, 235, 2971–2981.
pubmed: 28717819
doi: 10.1007/s00221-017-5027-z
Patton, J. H., Stanford, M. S., & Barratt, E. S. (1995). Factor structure of the Barratt impulsiveness scale. Journal of Clinical Psychology, 51, 768–774.
pubmed: 8778124
doi: 10.1002/1097-4679(199511)51:6<768::AID-JCLP2270510607>3.0.CO;2-1
Rae, C. L., Nombela, C., Rodriguez, P. V., Ye, Z., Hughes, L. E., Jones, P. S., Ham, T., Rittman, T., Coyle-Gilchrist, I., Regenthal, R., Sahakian, B. J., Barker, R. A., Robbins, T. W., & Rowe, J. B. (2016). Atomoxetine restores the response inhibition network in Parkinson’s disease. Brain, 139, 2235–2248.
pubmed: 27343257
pmcid: 4958901
doi: 10.1093/brain/aww138
Ray Li, C. S., Yan, P., Sinha, R., Lee, T. W., Li, C. S., Yan, P., Sinha, R., & Lee, T. W. (2008). Subcortical processes of motor response inhibition during a stop signal task. NeuroImage, 41, 1352–1363.
doi: 10.1016/j.neuroimage.2008.04.023
Rubia, K., Smith, A. B., Brammer, M. J., & Taylor, E. (2003). Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. NeuroImage, 20, 351–358.
pubmed: 14527595
doi: 10.1016/S1053-8119(03)00275-1
Rubia, K., Smith, A. B., Taylor, E., & Brammer, M. (2007). Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes. Human Brain Mapping, 28, 1163–1177.
pubmed: 17538951
pmcid: 6871440
doi: 10.1002/hbm.20347
Schmidt, R., Leventhal, D. K., Mallet, N., Chen, F., & Berke, J. D. (2013). Canceling actions involves a race between basal ganglia pathways. Nature Neuroscience, 16, 1118–1124.
pubmed: 23852117
pmcid: 3733500
doi: 10.1038/nn.3456
Swick, D., Ashley, V., & Turken, A. U. (2008). Left inferior frontal gyrus is critical for response inhibition. BMC Neuroscience, 9, 102.
pubmed: 18939997
pmcid: 2588614
doi: 10.1186/1471-2202-9-102
Verbruggen F, Aron AR, Band GP, Beste C, Bissett PG, Brockett AT, Brown JW, Chamberlain SR, Chambers CD, Colonius H, Colzato LS, Corneil BD, Coxon JP, Dupuis A, Eagle DM, Garavan H, Greenhouse I, Heathcote A, Huster RJ, Jahfari S, Kenemans JL, Leunissen I, Li C-SR, Logan GD, Matzke D, Morein-Zamir S, Murthy A, Paré M, Poldrack RA, Ridderinkhof KR, Robbins TW, Roesch M, Rubia K, Schachar RJ, Schall JD, Stock A-K, Swann NC, Thakkar KN, van der Molen MW, Vermeylen L, Vink M, Wessel JR, Whelan R, Zandbelt BB, Boehler CN (2019). A consensus guide to capturing the ability to inhibit actions and impulsive behaviors in the stop-signal task. Elife, 29, 8:e46323.
Vriend, C., Gerrits, N. J. H. M., Berendse, H. W., Veltman, D. J., van den Heuvel, O., & a., van der Werf YD,. (2015). Failure of stop and go in de novo Parkinson’s disease–a functional magnetic resonance imaging study. Neurobiology of Aging, 36, 470–475.
pubmed: 25150576
doi: 10.1016/j.neurobiolaging.2014.07.031
Ye, Z., Altena, E., Nombela, C., Housden, C. R., Maxwell, H., Rittman, T., Huddleston, C., Rae, C. L., Regenthal, R., Sahakian, B. J., Barker, R. A., Robbins, T. W., & Rowe, J. B. (2014a). Improving Response Inhibition in Parkinson’s Disease with Atomoxetine. Biological Psychiatry, 77(8), 740–748.
pubmed: 24655598
doi: 10.1016/j.biopsych.2014.01.024
Ye, Z., Altena, E., Nombela, C., Housden, C. R., Maxwell, H., Rittman, T., Huddleston, C., Rae, C. L., Regenthal, R., Sahakian, B. J., Barker, R. A., Robbins, T. W., & Rowe, J. B. (2014b). Selective serotonin reuptake inhibition modulates response inhibition in Parkinson’s disease. Brain, 137, 1145–1155.
pubmed: 24578545
pmcid: 3959561
doi: 10.1093/brain/awu032
Zandbelt, B. B., Bloemendaal, M., Hoogendam, J. M., Kahn, R. S., & Vink, M. (2013). Transcranial Magnetic Stimulation and Functional MRI Reveal Cortical and Subcortical Interactions during Stop-signal Response Inhibition. Journal of Cognitive Neuroscience, 25, 157–174.
pubmed: 23066733
doi: 10.1162/jocn_a_00309