Skip to main content Accessibility help
×
Home

Action Control Deficits in Patients With Essential Tremor

  • Shelby Hughes (a1), Daniel O. Claassen (a1), Wery P.M. van den Wildenberg (a2) (a3), Fenna T. Phibbs (a1), Elise B. Bradley (a1), Scott A. Wylie (a4) and Nelleke C. van Wouwe (a1) (a4)...

Abstract

Objectives: Essential tremor (ET) is a movement disorder characterized by action tremor which impacts motor execution. Given the disrupted cerebellar-thalamo-cortical networks in ET, we hypothesized that ET could interfere with the control mechanisms involved in regulating motor performance. The ability to inhibit or stop actions is critical for navigating many daily life situations such as driving or social interactions. The current study investigated the speed of action initiation and two forms of action control, response stopping and proactive slowing in ET. Methods: Thirty-three ET patients and 25 healthy controls (HCs) completed a choice reaction task and a stop-signal task, and measures of going speed, proactive slowing and stop latencies were assessed. Results: Going speed was significantly slower in ET patients (649 ms) compared to HCs (526 ms; F(1,56) = 42.37; p <.001; η2 = .43), whereas proactive slowing did not differ between groups. ET patients exhibited slower stop signal reaction times (320 ms) compared to HCs (258 ms, F(1,56) = 15.3; p <.00; η2 = .22) and more severe motor symptoms of ET were associated with longer stopping latencies in a subset of patients (Spearman rho = .48; p <.05). Conclusions: In line with previous studies, ET patients showed slower action initiation. Additionally, inhibitory control was impaired whereas proactive slowing remained intact relative to HCs. More severe motor symptoms of ET were associated with slower stopping speed, and may reflect more progressive changes to the cerebellar-thalamo-cortical network. Future imaging studies should specify which structural and functional changes in ET can explain changes in inhibitory action control. (JINS, 2019, 25, 156–164)

Copyright

Corresponding author

Correspondence and reprint requests to: Nelleke C. van Wouwe, Human Cognition and Neurophysiology Group, Department of Neurological Surgery, University of Louisville, 220 Abraham Flexner Way, 15th Floor, Louisville, KY 40202

References

Hide All
Alderson, R.M., Rapport, M.D., & Kofler, M.J. (2007). Attention-deficit/hyperactivity disorder and behavioral inhibition: A meta-analytic review of the stop-signal paradigm. Journal of Abnormal Child Psychology, 35(5), 745758. doi:10.1007/s10802-007-9131-6
Aron, A., Herz, D., Brown, P., Forstmann, B., & Zaghloul, K. (2016). Frontosubthalamic circuits for control of action and cognition. The Journal of Neuroscience, 36(45), 1148911495.
Bagepally, B.S., Bhatt, M.D., Chandran, V., Saini, J., Bharath, R.D., Vasudev, M.K., … Pal, P.K. (2012). Decrease in cerebral and cerebellar gray matter in essential tremor: A voxel-based morphometric analysis under 3T MRI. Journal of Neuroimaging, 22(3), 275278. doi:10.1111/j.1552-6569.2011.00598.x
Band, G.P.H., van der Molen, M.W., & Logan, G.D. (2003). Horse-race model simulations of the stop-signal procedure. Acta Psychologica, 112(2), 105142.
Bartoli, E., Aron, A.R., & Tandon, N. (2018). Topography and timing of activity in right inferior frontal cortex and anterior insula for stopping movement. Human Brain Mapping, 39(1), 189203.
Beck, A.T., Steer, R.A., & Brown, G.K. (1996). Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.
Benito-León, J., Louis, E., Romero, J., Hernández-Tamames, J., Manzanedo, E., Álvarez-Linera, J., … Onofrj., M. (2015). Altered functional connectivity in essential tremor. Medicine (Baltimore), 94(49), e1936.
Benito-León, J., & Louis, E.D. (2006). Essential tremor: Emerging views of a common disorder. Nature Clinical Practice. Neurology, 2(12), 666678
Bhalsing, K., Upadhyay, N., Kumar, K., Saini, J., Yadav, R., Gupta, A., & Pal, P. (2014). Association between cortical volume loss and cognitive impairments in essential tremor. European Journal of Neurology, 21(6), 874883.
Bissett, P.G., & Logan, G.D. (2011). Balancing cognitive demands: Control adjustments in the stop-signal paradigm. Journal of Experimental Psychology. Learning, Memory, and Cognition, 37(2), 392404. doi:10.1037/a0021800
Brunamonti, E., Chiricozzi, F.R., Clausi, S., Olivito, G., Giusti, M.A., Molinari, M., … Leggio, M. (2014). Cerebellar damage impairs executive control and monitoring of movement generation. PLoS One, 9(1), e85997. doi:10.1371/journal.pone.0085997
Cai, W., Ryali, S., Chen, T., Li, C.S., & Menon, V. (2014). Dissociable roles of right inferior frontal cortex and anterior insula in inhibitory control: Evidence from intrinsic and task-related functional parcellation, connectivity, and response profile analyses across multiple datasets. The Journal of Neuroscience, 34(44), 1465214667.
Cerasa, A., & Quattrone, A. (2016). Linking essential tremor to the cerebellum-neuroimaging evidence. Cerebellum, 15(3), 263275. doi:10.1007/s12311-015-0739-8
Delis, D.C., Kaplan, E., and Kramer, J. 2001. Delis Kaplan Executive Function System. San Antonio, TX: The Psychological Corporation.
Fahn, S., Tolosa, E., & Marín, C. (1988). Clinical rating scale for tremor. In J. Jankovic, & E. Tolosa (Eds.), Parkinson’s disease and movement disorders (pp. 225234). Baltimore: Urban and Schwarzenberg.
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, 189198.
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(3), 13131319.
Heldman, D., Jankovic, J., Vaillancourt, D., Prodoehl, J., Elble, R., & Giuffrida, J. (2011). Essential tremor quantification during activities of daily living. Parkinsonism & Related Disorders, 17(7), 537542. doi:10.1016/j.parkreldis.2011.04.017
Hirose, S., Jimura, K., Kunimatsu, A., Abe, O., Ohtomo, K., Miyashita, Y., & Konishi, S. (2014). Changes in cerebro-cerebellar interaction during response inhibition after performance improvement. Neuroimage, 99, 142148. doi:10.1016/j.neuroimage.2014.05.007
Hübner, J., Sprenger, A., Klein, C., Hagenah, J., Rambold, H., Zühlke, C., … Helmchen, C. (2007). Eye movement abnormalities in spinocerebellar ataxia type 17 (SCA17). Neurology, 69(11), 11601168. doi:10.1212/01.wnl.0000276958.91986.89
Hung, Y., Gaillard, S.L., Yarmak, P., & Arsalidou, M. (2018). Dissociations of cognitive inhibition, response inhibition, and emotional interference: Voxelwise ALE meta-analyses of fMRI studies. Human Brain Mapping, 39, 40654082.
Kay, G.G., Schwartz, H.I., Wingertzahn, M.A., Jayawardena, S., & Rosenberg, R.P. (2016). Next-day residual effects of gabapentin, diphenhydramine, and triazolam on simulated driving performance in healthy volunteers: A phase 3, randomized, double-blind, placebo-controlled, crossover trial. Human Psychopharmacology, 31(3), 217226. doi:10.1002/hup.2530
Kunimatsu, J., Suzuki, T.W., & Tanaka, M. (2016). Implications of lateral cerebellum in proactive control of saccades. The Journal of Neuroscience, 36(26), 70667074. doi:10.1523/JNEUROSCI.0733-16.2016
Leroi, I., McDonald, K., Pantula, H., & Harbishettar, V. (2012). Cognitive impairment in Parkinson disease: Impact on quality of life, disability, and caregiver burden. Journal of Geriatric Psychiatry and Neurology, 25(4), 208214. doi:10.1177/0891988712464823
Levitt, H. (1971). Transformed up-down methods in psychoacoustics. The Journal of the Acoustical Society of America, 49(Suppl. 2), 467477.
Lipszyc, J., & Schachar, R. (2010). Inhibitory control and psychopathology: A meta-analysis of studies using the Stop-Signal task. Journal of the International Neuropsychological Society, 16, 10641076.
Logan, G.D. (1994). Spatial attention and the apprehension of spatial relations. Journal of Experimental Psychology: Human Perception and Performance, 20, 10151036.
Louis, E.D. (2009). Essential tremors: A family of neurodegenerative disorders? Archives of Neurology, 66(10), 12021208. doi:10.1001/archneurol.2009.217
Louis, E.D., Ottman, R., Ford, B., Pullman, S., Martinez, M., Fahn, S., & Hauser, W.A. (1997). The Washington Heights-Inwood Genetic Study of Essential Tremor: Methodologic issues in essential-tremor research. Neuroepidemiology, 16(3), 124133.
Manza, P., Amandola, M., Tatineni, V., Li, C.R., & Leung, H.C. (2017). Response inhibition in Parkinson’s disease: A meta-analysis of dopaminergic medication and disease duration effects. NPJ Parkinson’s Disease, 3, 23. doi:10.1038/s41531-017-0024-2
Mirabella, G., Pani, P., & Ferraina, S. (2011). Neural correlates of cognitive control of reaching movements in the dorsal premotor cortex of rhesus monkeys. Journal of Neurophysiology, 106(3), 14541466. doi:10.1152/jn.00995.2010
Olivito, G., Brunamonti, E., Clausi, S., Pani, P., Chiricozzi, F.R., Giamundo, 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(10), 29712981. doi:10.1007/s00221-017-5027-z
O’Muircheartaigh, J., Keller, S.S., Barker, G.J., & Richardson, M.P. (2015). White matter connectivity of the thalamus delineates the functional architecture of competing thalamocortical systems. Cerebral Cortex, 25(11), 44774489.
Pauletti, C., Mannarelli, D., De Lucia, M.C., Locuratolo, N., Currà, A., Missori, P., … Fattapposta, F. (2015). Selective attentional deficit in essential tremor: Evidence from the attention network test. Parkinsonism & Related Disorders, 21(11), 13061311. doi:10.1016/j.parkreldis.2015.08.035
Randolph, C., Tierney, M.C., Mohr, E., & Chase, T.N. (1998). The Repeatable Battery for the Assessment of Neuropsychological Status (RBANS): Preliminary clinical validity. Journal of Clinical and Experimental Neuropsychology, 20(3), 310319.
Schnitzler, A., Münks, C., Butz, M., Timmermann, L., & Gross, J. (2009). Synchronized brain network associated with essential tremor as revealed by magnetoencephalography. Movement Disorders, 24(11), 16291635.
Sun, C., Wang, Y., Cui, R., Wu, C., Li, X., & Bao, Y. (2018). Human thalamic-prefrontal peduncle connectivity revealed by diffusion spectrum imaging fiber tracking. Frontiers in Neuroanatomy, 12, 24.
Swick, D., Ashley, V., & Turken, U. (2011). Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks. Neuroimage, 56(3), 16551665.
Tröster, A., Woods, S., Fields, J., Lyons, K., Pahwa, R., Higginson, C., & Koller, W. (2002). Neuropsychological deficits in essential tremor: An expression of cerebello‐thalamo‐cortical pathophysiology? European Journal of Neurology, 9(2), 143151.
van den Wildenberg, W.P.M., van Boxtel, G.J.M., van der Molen, M.W., Bosch, D.A., Speelman, J.D., & Brunia, C.H.M. (2006). Stimulation of the subthalamic region facilitates the selection and inhibition of motor responses in Parkinson’s disease. Journal of Cognitive Neuroscience, 18, 626636.
van Wouwe, N.C., van den Wildenberg, W.P., Claassen, D.O., Kanoff, K., Bashore, T.R., & Wylie, S.A. (2014). Speed pressure in conflict situations impedes inhibitory action control in Parkinson’s disease. Biological Psychology, 101, 4460. doi:10.1016/j.biopsycho.2014.07.002
Wylie, S.A., Claassen, D.O., Kanoff, K.E., van Wouwe, N.C., & van den Wildenberg, W.P. (2016). Stopping manual and vocal actions in Tourette’s syndrome. The Journal of Neuropsychiatry and Clinical Neurosciences, appineuropsych15110387. doi:10.1176/appi.neuropsych.15110387
Wylie, S.A., van den Wildenberg, W.P., Ridderinkhof, K.R., Bashore, T.R., Powell, V.D., Manning, C.A., & Wooten, G.F. (2009). The effect of speed-accuracy strategy on response interference control in Parkinson’s disease. Neuropsychologia, 47(8–9), 18441853. doi:10.1016/j.neuropsychologia.2009.02.025

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed