Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T07:12:12.508Z Has data issue: false hasContentIssue false
  • English
  • Français

Motivational Sensitivities Linked to Impulsive Motor Errors in Parkinson’s Disease

Published online by Cambridge University Press:  22 August 2017

Richard Laurent ,
Nelleke Corine van Wouwe ,
Maxim Turchan ,
Christopher Tolleson ,
Fenna Phibbs ,
Elise Bradley ,
Wery van den Wildenberg  and
Scott A. Wylie
Richard Laurent*
Affiliation:
Department of Neurology, University of Iowa Hospitals and Clinics, Iowa City, Iowa
Nelleke Corine van Wouwe
Affiliation:
Department of Neurology, Vanderbilt University Medical Center, Nashville, Tennessee
Maxim Turchan
Affiliation:
Department of Neurology, Vanderbilt University Medical Center, Nashville, Tennessee
Christopher Tolleson
Affiliation:
Department of Neurology, Vanderbilt University Medical Center, Nashville, Tennessee
Fenna Phibbs
Affiliation:
Department of Neurology, Vanderbilt University Medical Center, Nashville, Tennessee
Elise Bradley
Affiliation:
Department of Neurology, Vanderbilt University Medical Center, Nashville, Tennessee
Wery van den Wildenberg
Affiliation:
Amsterdam Brain and Cognition (ABC) and Psychology Department, University of Amsterdam, Amsterdam, The Netherlands
Scott A. Wylie
Affiliation:
Department of Neurosurgery, University of Louisville, Louisville, Kentucky
*
Correspondence and reprint requests to: Richard L. Laurent, 200 Hawkins Drive, 0120Z Roy Carver Pavilion, Department of Neurology-Neuropsychology, University of Iowa Hospitals and Clinics, Iowa City, Iowa 52242. E-mail: richard-laurent@uiowa.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: We investigated how broad motivational tendencies are related to the expression and suppression of action impulses in Parkinson’s disease (PD). Methods: Sixty-nine participants with PD completed a Simon response conflict task and Behavioral Inhibition System (BIS) and Behavioral Activation System (BAS) scales based on Gray’s (1987) reinforcement sensitivity theory. Analyses determined relationships between BIS, BAS, and the susceptibility to making impulsive action errors and the proficiency of inhibiting interference from action impulses. Results:BIS scores correlated positively with rates of impulsive action errors, indicating that participants endorsing low BIS tendencies were much more susceptible to acting on strong motor impulses. Analyses of subgroups with high versus low BIS scores confirmed this pattern and ruled out alternative explanations in terms of group differences in speed-accuracy tradeoffs. None of the scores on the BIS or BAS scales correlated with reactive inhibitory control. Conclusions: PD participants who endorse diminished predilection toward monitoring and avoiding aversive experiences (low BIS) show much greater difficulty restraining fast, impulsive motor errors. Establishing relationships between motivational sensitivities and cognitive control processes may have important implications for treatment strategies and positive health outcomes in participants with PD, particularly those at risk for falling and driving difficulties related to impulsive reactions. (JINS, 2018, 24, 128–138)

Keywords

InhibitionCognitionArousalRewardPunishmentIndividuality
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 24 , Issue 2 , February 2018 , pp. 128 - 138
Copyright
Copyright © The International Neuropsychological Society 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amodio, D.M., Master, S.L., Yee, C.M., & Taylor, S.E. (2008). Neurocognitive components of the behavioral inhibition and activation systems: Implications for theories of self‐regulation. Psychophysiology, 45(1), 11–19.Google Scholar
Balconi, M., Falbo, L., & Conte, V.A. (2012). BIS and BAS correlates with psychophysiological and cortical response systems during aversive and appetitive emotional stimuli processing. Motivation and Emotion, 36(2), 218–231.Google Scholar
Beck, A.T., Steer, R.A., & Brown, G.K. (1996). Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.Google Scholar
Berkman, E.T., Lieberman, M.D., & Gable, S.L. (2009). BIS, BAS, and response conflict: Testing predictions of the revised reinforcement sensitivity theory. Personality and Individual Differences, 46(5), 586–591.Google Scholar
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), 392–404.Google Scholar
Botvinick, M.M., Braver, T.S., Barch, D.M., Carter, C.S., & Cohen, J.D. (2001). Conflict monitoring and cognitive control. Psychological Review, 108(3), 624–652.Google Scholar
Bub, D.N., Masson, M.E., & Lalonde, C.E. (2006). Cognitive control in children Stroop interference and suppression of word reading. Psychological Science, 17(4), 351–357.Google Scholar
Burle, B., Possamaï, C.-A., Vidal, F., Bonnet, M., & Hasbroucq, T. (2002). Executive control in the Simon effect: An electromyographic and distributional analysis. Psychological Research, 66(4), 324–336.Google Scholar
Carter, C.S., Braver, T.S., Barch, D.M., Botvinick, M.M., Noll, D., & Cohen, J.D. (1998). Anterior cingulate cortex, error detection, and the online monitoring of performance. Science, 280(5364), 747–749.Google Scholar
Carver, C.S., & White, T.L. (1994). Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS scales. Journal of Personality and Social Psychology, 67(2), 319.Google Scholar
Claassen, D.O., & Wylie, S.A. (2012). Trends and issues in characterizing early cognitive changes in Parkinson’s disease. Current Neurology and Neuroscience Reports, 12(6), 695–702.Google Scholar
Cooper, J.A., Sagar, H.J., Tidswell, P., & Jordan, N. (1994). Slowed central processing in simple and go/no-go reaction time tasks in Parkinson’s disease. Brain, 117(3), 517–529.Google Scholar
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(3), 189–198.Google Scholar
Gauggel, S., Rieger, M., & Feghoff, T. (2004). Inhibition of ongoing responses in patients with Parkinson’s disease. Journal of Neurology, Neurosurgery, & Psychiatry, 75(4), 539–544.Google Scholar
Goetz, C.G., Tilley, B.C., Shaftman, S.R., Stebbins, G.T., Fahn, S., Martinez‐Martin, P., & Dodel, R. (2008). Movement Disorder Society‐sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS‐UPDRS): Scale presentation and clinimetric testing results. Movement Disorders, 23(15), 2129–2170.Google Scholar
Gomez, R., & Corr, P.J. (2014). ADHD and personality: A meta-analytic review. Clinical Psychology Review, 34(5), 376–388.Google Scholar
Gray, J.A. (1982). On mapping anxiety. Behavioral and Brain Sciences, 5(3), 506–534.CrossRefGoogle Scholar
Gray, J.A. (1987). The neuropsychology of emotion and personality. In S.M. Stahl, S.D. Iversen & E.C. Goodman (Eds.), Cognitive neurochemistry (Vol. xiv, pp. 171–190). New York, NY: Oxford University Press.Google Scholar
Gray, J.A., & McNaughton, N. (2000). The neuropsychology of anxiety: An enquiry into the function of the septo-hippocampal system. New York: Oxford University Press.Google Scholar
Hershey, T., Campbell, M.C., Videen, T.O., Lugar, H.M., Weaver, P.M., Hartlein, J., & Perlmutter, J.S. (2010). Mapping go–no-go performance within the subthalamic nucleus region. Brain, 133(12), 3625–3634.Google Scholar
Heym, N., Kantini, E., Checkley, H.L.R., & Cassaday, H.J. (2015). Gray’s revised reinforcement sensitivity theory in relation to attention-deficit/hyperactivity and tourette-like behaviors in the general population. Personality and Individual Differences, 78, 24–28.Google Scholar
Hoehn, M.M., & Yahr, M.D. (1998). Parkinsonism: Onset, progression, and mortality. Neurology, 50(2), 318–318.Google Scholar
Ishihara, L., & Brayne, C. (2006). A systematic review of depression and mental illness preceding Parkinson’s disease. Acta Neurologica Scandinavica, 113(4), 211–220.CrossRefGoogle ScholarPubMed
Johnson, S.L., Turner, R.J., & Iwata, N. (2003). BIS/BAS levels and psychiatric disorder: An epidemiological study. Journal of Psychopathology and Behavioral Assessment, 25(1), 25–36.Google Scholar
Kehagia, A.A., Housden, C.R., Regenthal, R., Barker, R.A., Müller, U., Rowe, J., & Robbins, T.W. (2014). Targeting impulsivity in Parkinson’s disease using atomoxetine. Brain, 137(7), 1986–1997.Google Scholar
Kornblum, S., Hasbroucq, T., & Osman, A. (1990). Dimensional overlap: Cognitive basis for stimulus-response compatibility--A model and taxonomy. Psychological Review, 97(2), 253.CrossRefGoogle ScholarPubMed
Lewis, S.J., & Shine, J.M. (2014). The next step: A common neural mechanism for freezing of gait. The Neuroscientist, 22(1), 72–82.Google Scholar
Luce, R.D. (1991). Response times: Their role in inferring elementary mental organization. New York: Oxford University Press.Google Scholar
Maack, D.J., Tull, M.T., & Gratz, K.L. (2012). Examining the incremental contribution of behavioral inhibition to generalized anxiety disorder relative to other Axis I disorders and cognitive-emotional vulnerabilities. Journal of Anxiety Disorders, 26(6), 689–695.Google Scholar
McNaughton, N., & Corr, P.J. (2004). A two-dimensional neuropsychology of defense: Fear/anxiety and defensive distance. Neuroscience & Biobehavioral Reviews, 28(3), 285–305.Google Scholar
Nutt, J.G., Bloem, B.R., Giladi, N., Hallett, M., Horak, F.B., & Nieuwboer, A. (2011). Freezing of gait: Moving forward on a mysterious clinical phenomenon. The Lancet Neurology, 10(8), 734–744.Google Scholar
Obeso, I., Wilkinson, L., & Jahanshahi, M. (2011). Levodopa medication does not influence motor inhibition or conflict resolution in a conditional stop-signal task in Parkinson’s disease. Experimental Brain Research, 213(4), 435.Google Scholar
Praamstra, P., & Plat, F.M. (2001). Failed suppression of direct visuomotor activation in Parkinson’s disease. Journal of Cognitive Neuroscience, 13(1), 31–43.Google Scholar
Proctor, R.W., Miles, J.D., & Baroni, G. (2011). Reaction time distribution analysis of spatial correspondence effects. Psychonomic Bulletin & Review, 18(2), 242–266.Google Scholar
Reuter, M., Schmitz, A., Corr, P., & Hennig, J. (2007). Molecular genetics support Gray’s personality theory: The interaction of COMT and DRD2 polymorphisms predicts the behavioural approach system. The International Journal of Neuropsychopharmacology, 10(1), 1–12.Google Scholar
Ridderinkhof, K.R., Forstmann, B.U., Wylie, S.A., Burle, B., & van den Wildenberg, W.P. (2011). Neurocognitive mechanisms of action control: Resisting the call of the Sirens. Wiley Interdisciplinary Reviews: Cognitive Science, 2(2), 174–192.Google Scholar
Ridderinkhof, K.R., Scheres, A., Oosterlaan, J., & Sergeant, J.A. (2005). Delta plots in the study of individual differences: New tools reveal response inhibition deficits in ADHD that are eliminated by methylphenidate treatment. Journal of Abnormal Psychology, 114(2), 197–215.Google Scholar
Ridderinkhof, K.R., Van Den Wildenberg, W.P., Segalowitz, S.J., & Carter, C.S. (2004). Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain and Cognition, 56(2), 129–140.Google Scholar
Ridderinkhof, R.K. (2002). Micro-and macro-adjustments of task set: Activation and suppression in conflict tasks. Psychological Research, 66(4), 312–323.CrossRefGoogle ScholarPubMed
Shackman, A.J., McMenamin, B.W., Maxwell, J.S., Greischar, L.L., & Davidson, R.J. (2009). Right dorsolateral prefrontal cortical activity and behavioral inhibition. Psychological Science, 20(12), 1500–1506.Google Scholar
Shinagawa, S., Babu, A., Sturm, V., Shany-Ur, T., Toofanian Ross, P., Zackey, D., & Rankin, K.P. (2015). Neural basis of motivational approach and withdrawal behaviors in neurodegenerative disease. Brain and Behavior, 5(9), e00350.Google Scholar
Simon, J.R. (1969). Reactions toward the source of stimulation. Journal of Experimental Psychology, 81(1), 174–176.CrossRefGoogle ScholarPubMed
Sommer, K., Van Der Molen, M.W., & De Pascalis, V. (2016). BIS/BAS sensitivity and emotional modulation in a prepulse-inhibition paradigm: A brain potential study. Physiology & Behavior, 154, 100–113.Google Scholar
Sütterlin, S., Andersson, S., & Claus, V. (2011). Inhibition in action-inhibitory components in the behavioral activation system. Journal of Behavioral and Brain Science, 1(3), 160–166.Google Scholar
Todes, C.J., & Lees, A.J. (1985). The pre-morbid personality of patients with Parkinson’s disease. Journal of Neurology, Neurosurgery, & Psychiatry, 48(2), 97–100.Google Scholar
van Den Wildenberg, W.P., Wylie, S.A., Forstmann, B.U., Burle, B., Hasbroucq, T., & Ridderinkhof, K.R. (2010). To head or to heed? Beyond the surface of selective action inhibition: A review. Frontiers in Human Neuroscience, 4, 222.Google Scholar
van Steenbergen, H., Band, G.P., & Hommel, B. (2009). Reward counteracts conflict adaptation evidence for a role of affect in executive control. Psychological Science, 20(12), 1473–1477.Google Scholar
van Wouwe, N., van den Wildenberg, W., Claassen, D., Kanoff, K., Bashore, T., & Wylie, S. (2014). Speed pressure in conflict situations impedes inhibitory action control in Parkinson’s disease. Biological Psychology, 101, 44–60.Google Scholar
van Wouwe, N.C., Kanoff, K.E., Claassen, D.O., Spears, C.A., Neimat, J., van den Wildenberg, W.P., & Wylie, S.A. (2016). Dissociable effects of dopamine on the initial capture and the reactive inhibition of impulsive actions in Parkinson’s disease. Journal of Cognitive Neuroscience, (5), 710–723.Google Scholar
Vandenbossche, J., Deroost, N., Soetens, E., Coomans, D., Spildooren, J., Vercruysse, S., & Kerckhofs, E. (2013). Freezing of gait in Parkinson’s disease: Disturbances in automaticity and control. Frontiers in Human Neuroscience, 6, 356.Google Scholar
Verbruggen, F., & Logan, G.D. (2008). Response inhibition in the stop-signal paradigm. Trends in Cognitive Sciences, 12(11), 418–424.Google Scholar
Weintraub, D., Siderowf, A.D., Potenza, M.N., Goveas, J., Morales, K.H., Duda, J.E., & Stern, M.B. (2006). Association of dopamine agonist use with impulse control disorders in Parkinson disease. Archives of Neurology, 63(7), 969–973.Google Scholar
Wijnen, J.G., & Ridderinkhof, K.R. (2007). Response inhibition in motor and oculomotor conflict tasks: Different mechanisms, different dynamics? Brain and Cognition, 63(3), 260–270.Google Scholar
Wylie, S., Van Den Wildenberg, W., Ridderinkhof, K., Bashore, T., Powell, V., Manning, C., & Wooten, G. (2009a). The effect of speed-accuracy strategy on response interference control in Parkinson’s disease. Neuropsychologia, 47(8), 1844–1853.Google Scholar
Wylie, S., van den Wildenberg, W., Ridderinkhof, K., Bashore, T., Powell, V., Manning, C., & Wooten, G. (2009b). The effect of Parkinson’s disease on interference control during action selection. Neuropsychologia, 47(1), 145–157.Google Scholar
Wylie, S.A., Ridderinkhof, K.R., Bashore, T.R., & van den Wildenberg, W.P. (2010). The effect of Parkinson’s disease on the dynamics of on-line and proactive cognitive control during action selection. Journal of Cognitive Neuroscience, 22(9), 2058–2073.Google Scholar
Wylie, S.A., Ridderinkhof, K.R., Elias, W.J., Frysinger, R.C., Bashore, T.R., Downs, K.E., & van den Wildenberg, W.P. (2010). Subthalamic nucleus stimulation influences expression and suppression of impulsive behaviour in Parkinson’s disease. Brain, 133, 3611–3624.Google Scholar
Wylie, S.A., van den Wildenberg, W., Ridderinkhof, K.R., Claassen, D.O., Wooten, G.F., & Manning, C.A. (2012). Differential susceptibility to motor impulsivity among functional subtypes of Parkinson’s disease. Journal of Neurology, Neurosurgery, & Psychiatry, 83(12), 1149–1154.Google Scholar
Ye, Z., Rae, C.L., Nombela, C., Ham, T., Rittman, T., Jones, P.S., & Housden, C.R. (2016). Predicting beneficial effects of atomoxetine and citalopram on response inhibition in Parkinson’s disease with clinical and neuroimaging measures. Human Brain Mapping, 37(3), 1026–1037.CrossRefGoogle ScholarPubMed
Yeung, N., Botvinick, M.M., & Cohen, J.D. (2004). The neural basis of error detection: Conflict monitoring and the error-related negativity. Psychological Review, 111(4), 931–959.Google Scholar