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Parkinson’s Disease Subtypes Show Distinct Tradeoffs Between Response Initiation and Inhibition Latencies

Published online by Cambridge University Press:  15 June 2017

Christopher Tolleson*
Affiliation:
Department of Neurology, Movement Disorders Division, Vanderbilt University, Nashville, Tennessee
Maxim Turchan
Affiliation:
Department of Neurology, Cognitive Division, Vanderbilt University, Nashville, Tennessee
Nelleke van Wouwe
Affiliation:
Department of Neurology, Cognitive Division, Vanderbilt University, Nashville, Tennessee
David Isaacs
Affiliation:
Department of Neurology, Movement Disorders Division, Vanderbilt University, Nashville, Tennessee
Fenna Phibbs
Affiliation:
Department of Neurology, Movement Disorders Division, Vanderbilt University, Nashville, Tennessee
Scott Wylie
Affiliation:
Department of Neurology, Cognitive Division, Vanderbilt University, Nashville, Tennessee
*
Correspondence and reprint requests to: Christopher Tolleson, Vanderbilt University, 1161 21st Avenue South, Medical Center North A-0118, Nashville, TN 37232. E-mail: christopher.tolleson@vanderbilt.edu

Abstract

Objectives: In unpredictable situations, individuals often show tradeoffs between response initiation and inhibition speeds. We tested the hypothesis that Parkinson’s disease (PD) motor subtypes differentially impact tradeoffs between these two action-oriented processes. We predicted that, compared to tremor dominant (TD) patients, predominant postural instability and gait dysfunction (PIGD) patients would show exacerbated tradeoffs between response initiation and inhibition in situations requiring the sudden potential need to interrupt an action. Methods: Fifty-one PD patients (subdivided into PIGD [n=27] and TD [n=24]) and 21 healthy controls (HCs) completed a choice reaction task to establish baseline response initiation speed between groups. Subsequently, participants completed a stop-signal task which introduced an occasional, unpredictable stop stimulus. We measured changes in initiation speed in preparation of an unpredictable stop (i.e., proactive slowing) and inhibition latency (i.e., stop-signal reaction time). Results: Compared to HCs, PD patients showed slower response initiation speeds in the choice reaction task. All groups showed proactive slowing in the stop-signal task but the magnitude was considerably larger in PIGD patients, almost twice as large as TD patients. PD patients, irrespective of motor subtype, showed longer inhibition latencies than HCs. Conclusions: PIGD and TD subtypes both showed exacerbated response inhibition deficits. However, PIGD patients showed much more pronounced proactive slowing in situations with an expected yet unpredictable need to stop action abruptly. This suggests that PIGD is accompanied by exaggerated tradeoffs between response initiation and inhibition processes to meet situational action demands. We discuss putative neural mechanisms and clinical implications of these findings. (JINS, 2017, 23, 665–674)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2017 

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References

REFERENCES

Alves, G., Larsen, J.P., Emre, M., Wentzel-Larsen, T., & Aarsland, D. (2006). Changes in motor subtype and risk for incident dementia in Parkinson’s disease. Movement Disorders, 21(8), 11231130.CrossRefGoogle ScholarPubMed
Aron, A.R. (2011). From reactive to proactive and selective control: Developing a richer model for stopping inappropriate responses. Biological Psychiatry, 69(12), e55e68.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Bissett, P.G., & Logan, G.D. (2012). Post-stop-signal adjustments: Inhibition improves subsequent inhibition. Journal of Experimental Psychology. Learning, Memory, and Cognition, 38(4), 955966.CrossRefGoogle ScholarPubMed
Bissett, P.G., Logan, G.D., van Wouwe, N.C., Tolleson, C.M., Phibbs, F.T., Claassen, D.O., && Wylie, S.A. (2015). Generalized motor inhibitory deficit in Parkinson’s disease patients who freeze. Journal of Neural Transmission, 122(12), 16931701. http://doi.org/10.1007/s00702-015-1454-9.CrossRefGoogle ScholarPubMed
Błaszczyk, J.W., Orawiec, R., Duda-Kłodowska, D., & Opala, G. (2007). Assessment of postural instability in patients with Parkinson’s disease. Experimental Brain Research, 183(1), 107114. http://doi.org/10.1007/s00221-007-1024-y.CrossRefGoogle ScholarPubMed
Claassen, D.O., van den Wildenberg, W.P., Harrison, M.B., van Wouwe, N.C., Kanoff, K., Neimat, J.S., && Wylie, S.A. (2015). Proficient motor impulse control in Parkinson disease patients with impulsive and compulsive behaviors. Pharmacology, Biochemistry, and Behavior, 129, 1925. doi: 10.1016/j.pbb.2014.11.017 CrossRefGoogle ScholarPubMed
Forstmann, B.U., Dutilh, G., Brown, S., Neumann, J., von Cramon, D.Y., Ridderinkhof, K.R., && Wagenmakers, E.J. (2008). Striatum and pre-SMA facilitate decision-making under time pressure. Proceedings of the National Academy of Sciences of the United States of America, 105(45), 1753817542. doi: 10.1073/pnas.0805903105 CrossRefGoogle Scholar
Frank, M.J. (2006). Hold your horses: A dynamic computational role for the subthalamic nucleus in decision making. Neural Networks, 19(8), 11201136.CrossRefGoogle ScholarPubMed
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(4), 539544.CrossRefGoogle ScholarPubMed
Giladi, N., Kao, R., & Fahn, S. (1997). Freezing phenomenon in patients with parkinsonian syndromes. Movement Disorders, 12(3), 302305.CrossRefGoogle ScholarPubMed
Herb, J.N., Rane, S., Isaacs, D.A., Van Wouwe, N., Roman, O.C., Landman, B.A., & Claassen, D.O. (2016). Cortical implications of advancing age and disease duration in Parkinson’s disease patients with postural instability and gait dysfunction. Journal of Parkinson’s Disease, 6(2), 441451.CrossRefGoogle ScholarPubMed
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), 181184. http://doi.org/10.1136/jnnp.55.3.181.CrossRefGoogle ScholarPubMed
Jankovic, J., McDermott, M., Carter, J., Gauthier, S., Goetz, C., Golbe, L., & Shoulson, I. (1990). Variable expression of Parkinson’s disease: A base-line analysis of the DATATOP cohort. The Parkinson Study Group. Neurology, 40(10), 15291534.CrossRefGoogle ScholarPubMed
Janvin, C., Aarsland, D., Larsen, J.P., & Hugdahl, K. (2003). Neuropsychological profile of patients with Parkinson’s disease without dementia. Dementia and Geriatric Cognitive Disorders, 15(3), 126131.CrossRefGoogle ScholarPubMed
Kelly, V.E., & Shumway-Cook, A. (2014). The ability of people with Parkinson’s disease to modify dual-task performance in response to instructions during simple and complex walking tasks. Experimental Brain Research, 232(1), 263271. http://doi.org/10.1007/s00221-013-3737-4.CrossRefGoogle ScholarPubMed
Kenemans, J.L. (2015). Specific proactive and generic reactive inhibition. Neuroscience and Biobehavioral Reviews, 56, 115126. doi: 10.1016/j.neubiorev.2015.06.011 CrossRefGoogle ScholarPubMed
Kerr, G.K., Worringham, C.J., Cole, M.H., Lacherez, P.F., Wood, J.M., & Silburn, P.A. (2010). Predictors of future falls in Parkinson disease. Neurology, 75(2), 116124.CrossRefGoogle ScholarPubMed
Levitt, H. (1971). Transformed up-down methods in psychoacoustics. The Journal of the Acoustical Society of America, 49 (2), Suppl 2: 467477.CrossRefGoogle ScholarPubMed
Logan, G.D., Cowan, W.B., & Davis, K.A. (1984). On the ability to inhibit simple and choice reaction time responses: A model and a method. Journal of Experimental Psychology. Human Perception and Performance, 10(2), 276291.CrossRefGoogle Scholar
Logan, G.D. (1994). On the ability to inhibit thought and action: A users guide to the stop-signal paradigm. In D. Dagenbach & T.H. Carr (Eds.), Inhibitory processes in attention, memory, and language (pp. 189239). San Diego, CA: Academic Press.Google Scholar
Logan, G.D., Schachar, R.J., & Tannock, R. (1997). Impulsivity and inhibitory control. Psychological Science, 8(1), 6064.CrossRefGoogle Scholar
Logemann, H.N., Böcker, K.B., Deschamps, P.K., van Harten, P.N., Koning, J., Kemner, C., & Kenemans, J.L. (2017). Haloperidol 2 mg impairs inhibition but not visuospatial attention. Psychopharmacology (Berlin), 234(2), 235244. doi: 10.1007/s00213-016-4454-z CrossRefGoogle Scholar
Lyros, E., Messinis, L., & Papathanasopoulos, P. (2008). Does motor subtype influence neurocognitive performance in Parkinson’s disease without dementia? European Journal of Neurology, 15(3), 262267.CrossRefGoogle ScholarPubMed
Marras, C., & Lang, A. (2013). Parkinson’s disease subtypes: Lost in translation? Journal of Neurology, Neurosurgery, and Psychiatry, 84(4), 409415.CrossRefGoogle ScholarPubMed
Nachev, P., Wydell, H., O’Neill, K., Husain, M., & Kennard, C. (2007). The role of the pre-supplementary motor area in the control of action. Neuroimage, 36(Suppl 2), T155T163.CrossRefGoogle ScholarPubMed
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), 734744. http://doi.org/10.1016/S1474-4422(11)70143-0.CrossRefGoogle ScholarPubMed
Obeso, I., Wilkinson, L., Casabona, E., Bringas, M.L., Alvarez, M., Alvarez, L., & Jahanshahi, M. (2011). Deficits in inhibitory control and conflict resolution on cognitive and motor tasks in Parkinson’s disease. Experimental Brain Research, 212(3), 371384.CrossRefGoogle ScholarPubMed
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), 435445. doi: 10.1007/s00221-011-2793-x CrossRefGoogle Scholar
Oh, J.Y., Kim, Y.-S., Choi, B.H., Sohn, E.H., & Lee, A.Y. (2009). Relationship between clinical phenotypes and cognitive impairment in Parkinson’s disease (PD). Archives of Gerontology and Geriatrics, 49(3), 351354.CrossRefGoogle ScholarPubMed
Paulus, W., & Jellinger, K. (1991). The neuropathologic basis of different clinical subgroups of Parkinson’s disease. Journal of Neuropathology and Experimental Neurology, 50(6), 743755.CrossRefGoogle ScholarPubMed
Rajput, A.H., Voll, A., Rajput, M.L., Robinson, C.A., & Rajput, A. (2009). Course in Parkinson disease subtypes: A 39-year clinicopathologic study. Neurology, 73(3), 206212.CrossRefGoogle ScholarPubMed
Rosenberg-Katz, K., Herman, T., Jacob, Y., Giladi, N., Hendler, T., & Hausdorff, J.M. (2013). Gray matter atrophy distinguishes between Parkinson disease motor subtypes. Neurology, 80(16), 14761484.CrossRefGoogle ScholarPubMed
Schiess, M.C., Zheng, H., Soukup, V.M., Bonnen, J.G., & Nauta, H.J. (2000). Parkinson’s disease subtypes: Clinical classification and ventricular cerebrospinal fluid analysis. Parkinsonism & Related Disorders, 6(2), 6976.CrossRefGoogle ScholarPubMed
Sollinger, A.B., Goldstein, F.C., Lah, J.J., Levey, A.I., & Factor, S.A. (2010). Mild cognitive impairment in Parkinson’s disease: Subtypes and motor characteristics. Parkinsonism & Related Disorders, 16(3), 177180.CrossRefGoogle ScholarPubMed
Stebbins, G.T., Goetz, C.G., Burn, D.J., Jankovic, J., Khoo, T.K., & Tilley, B.C. (2013). How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: Comparison with the unified Parkinson’s disease rating scale. Movement Disorders, 28(5), 668670.CrossRefGoogle ScholarPubMed
Stefanova, E., Jecmenica Lukic, M., Ziropadja, L., Markovic, V., Stojkovic, T., Tomic, A., & Kostic, V. (2014). Attentional set-shifting in Parkinson’s disease patients with freezing of gait-acquisition and discrimination set learning deficits at the background? Journal of the International Neuropsychological Society, 20(9), 929936.CrossRefGoogle ScholarPubMed
Van Rooden, S.M., Visser, M., Verbaan, D., Marinus, J., & van Hilten, J.J. (2009). Patterns of motor and non-motor features in Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 80(8), 846850.CrossRefGoogle ScholarPubMed
van den Wildenberg, W.P., van Boxtel, G.J., van der Molen, M.W., Bosch, D.A., Speelman, J.D., & Brunia, C.H. (2006). Stimulation of the subthalamic region facilitates the selection and inhibition of motor responses in Parkinson’s disease. Journal of Cognitive Neuroscience, 18(4), 626636.CrossRefGoogle ScholarPubMed
van Wouwe, N.C., van den Wildenberg, W.P.M., 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.CrossRefGoogle ScholarPubMed
Vink, M., Kaldewaij, R., Zandbelt, B.B., Pas, P., & du Plessis, S. (2015). The role of stop-signal probability and expectation in proactive inhibition. The European Journal of Neuroscience, 41(8), 10861094. doi: 10.1111/ejn.12879 CrossRefGoogle ScholarPubMed
Verbaan, D., Marinus, J., Visser, M., van Rooden, S.M., Stiggelbout, A.M., Middelkoop, H.A.M., && van Hilten, J.J. (2007). Cognitive impairment in Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 78(11), 11821187.CrossRefGoogle ScholarPubMed
Watanabe, T., Hanajima, R., Shirota, Y., Tsutsumi, R., Shimizu, T., Hayashi, T., & Konishi, S. (2015). Effects of rTMS of pre-supplementary motor area on fronto basal ganglia network activity during stop-signal task. Journal of Neuroscience, 35(12), 48134823. doi: 10.1523/JNEUROSCI.3761-14.2015 CrossRefGoogle ScholarPubMed
Wessel, J.R., & Aron, A.R. (2013). Unexpected events induce motor slowing via a brain mechanism for action-stopping with global suppressive effects. The Journal of Neuroscience, 33(47), 1848118491. doi: 10.1523/JNEUROSCI.3456-13.2013 CrossRefGoogle Scholar
Wu, Y., Guo, X.-Y., Wei, Q.-Q., Ou, R.-W., Song, W., Cao, B., & Shang, H.-F. (2016). Non-motor symptoms and quality of life in tremor dominant vs postural instability gait disorder Parkinson’s disease patients. Acta Neurologica Scandinavica, 133(5), 330337.CrossRefGoogle ScholarPubMed
Wylie, S.A., van den Wildenberg, W.P.M., 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.CrossRefGoogle ScholarPubMed
Wylie, S.A., Ridderinkhof, K.R., Elias, W.J., Frysinger, R.C., Bashore, T.R., Downs, K.E., & van den Wildenberg, W.P.M. (2010). Subthalamic nucleus stimulation influences expression and suppression of impulsive behaviour in Parkinson’s disease. Brain: A Journal of Neurology, 133(Pt 12), 36113624.CrossRefGoogle ScholarPubMed
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, and Psychiatry, 83(12), 11491154.CrossRefGoogle ScholarPubMed
Zandbelt, B.B., & Vink, M. (2010). On the role of the striatum in response inhibition. PLoS One, 5(11), e13848. doi: 10.1371/journal.pone.0013848 CrossRefGoogle ScholarPubMed
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(2), 157174. doi: 10.1162/jocn_a_00309 CrossRefGoogle ScholarPubMed