Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-19T07:22:55.627Z Has data issue: false hasContentIssue false
  • English
  • Français

Neural basis for impaired time reproduction in Parkinson's disease: An fMRI study

Published online by Cambridge University Press:  12 February 2004

CATHERINE L. ELSINGER ,
STEPHEN M. RAO ,
JANICE L. ZIMBELMAN ,
NORMAN C. REYNOLDS ,
KAREN A. BLINDAUER  and
RAYMOND G. HOFFMANN
CATHERINE L. ELSINGER
Affiliation:
Medical College of Wisconsin, Milwaukee, Wisconsin
STEPHEN M. RAO
Affiliation:
Medical College of Wisconsin, Milwaukee, Wisconsin
JANICE L. ZIMBELMAN
Affiliation:
Medical College of Wisconsin, Milwaukee, Wisconsin Carroll College, Waukesha, Wisconsin
NORMAN C. REYNOLDS
Affiliation:
Medical College of Wisconsin, Milwaukee, Wisconsin
KAREN A. BLINDAUER
Affiliation:
Medical College of Wisconsin, Milwaukee, Wisconsin
RAYMOND G. HOFFMANN
Affiliation:
Medical College of Wisconsin, Milwaukee, Wisconsin
Get access Rights & Permissions [Opens in a new window]

Abstract

Studies involving brain-lesioned subjects have used the paced finger tapping (PFT) task to investigate the neural systems that govern motor timing. Patients with Parkinson's disease (PD), for example, demonstrate abnormal performance on the PFT, characterized by decreased accuracy and variability changes, suggesting that the basal ganglia may play a critical role in motor timing. Consistent with this hypothesis, an fMRI study of healthy participants demonstrated that the medial frontostriatal circuit (dorsal putamen, ventrolateral thalamus, SMA) correlated with explicit time-dependent components of the PFT task. In the current fMRI study, PD patients and healthy age-matched controls were imaged while performing the PFT. PD patients underwent 2 imaging sessions, 1 on and the other off dopamine supplementation. Relative to controls, PD patients were less accurate and showed greater variability on the PFT task relative to controls. No PFT performance differences were observed between the on and off medication states despite significantly greater motor symptoms on the Unified Parkinson's Disease Rating Scale (UPDRS) in the off medication state. Functional imaging results demonstrated decreased activation within the sensorimotor cortex (SMC), cerebellum, and medial premotor system in the PD patients compared to controls. With dopamine replacement, an increase in the spatial extent of activation was observed within the SMC, SMA, and putamen in the PD patients. These results indicate that impaired timing reproduction in PD patients is associated with reduced brain activation within motor and medial premotor circuits. Despite a lack of improvement in PFT performance, PD patient's brain activation patterns were partially “normalized” with dopamine supplementation. These findings could not be attributed to greater head movement artifacts or basal ganglia atrophy within the PD group. (JINS, 2003, 9, 1088–1098.)

Keywords

Parkinson's diseaseTime reproductionDopamine replacement therapyFunctional magnetic resonance imagingBasal gangliaSensorimotor cortexSupplementary motor area
Type
THEMATIC ARTICLES
Information
Journal of the International Neuropsychological Society , Volume 9 , Issue 7 , November 2003 , pp. 1088 - 1098
Copyright
© 2003 The International Neuropsychological Society

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

REFERENCES

Alexander, G.E., DeLong, M.R., & Strick, P.L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9, 357–381.Google Scholar
Bookheimer, S.Y., Strojwas, M.H., Cohen, M.S., Saunders, A.M., Pericak-Vance, M.A., Mazziotta, J.C., & Small, G.W. (2000). Patterns of brain activation in people at risk for Alzheimer's disease. New England Journal of Medicine, 343, 450–456.Google Scholar
Bower, J.M. (1997). Control of sensory data acquisition. In J.D. Schmahmann (Ed.), The cerebellum and cognition (pp. 489–513). San Diego, CA: Academic Press.
Brooks, D.J., Ibanez, V., Sawle, G.V., Quinn, N., Lees, A.J., Mathias, C.J., Bannister, R., Marsden, C.D., & Frackowiak, R.S. (1990). Differing patterns of striatal 18F-dopa uptake in Parkinson's disease, multiple system atrophy and progressive supranuclear palsy. Annals of Neurology, 28, 547–555.Google Scholar
Cox, R.W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173.Google Scholar
Cox, R.W. & Hyde, J.S. (1997). Software tools for analysis and visualization of fMRI data. NMR Biomedical, 10, 171–178.Google Scholar
Defer, G.L., Widner, H., Marie, R.M., Remy, P., & Levivier, M. (1999). Core assessment program for surgical interventional therapies in Parkinson's disease (CAPSIT-PD). Movement Disorders, 14, 572–584.Google Scholar
Desmond, J.E., Gabrieli, J.D.E., Wagner, A.D., Ginier, B.L., & Glover, G.H. (1997). Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. Journal of Neuroscience, 17, 9675–9685.Google Scholar
Doyon, J., Song, A.W., Karni, A., Lalonde, F., Adams, M.M., & Ungerleider, L.G. (2002). Experience-dependent changes in cerebellar contributions to motor sequence learning. Proceedings of the National Academy of Sciences, U.S.A, 99, 1017–1022.CrossRefGoogle Scholar
Fahn, S., Elton, R.L., & Members of the UPDRS Development Committee. (1987). The United Parkinson's Disease Rating Scale. In S. Fahn, C.D. Marsden, D.B. Calne, & M. Goldstein (Eds.), Recent developments in Parkinson's disease (pp. 153–164). Florham, NJ: Macmillan Health Care Information.
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). Mini-Mental State. Journal of Psychiatric Research, 12, 189–198.Google Scholar
Forman, S.D., Cohen, J.D., Fitzgerald, M., Eddy, W.F., Mintun, M.A., & Knoll, D.C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of cluster-size threshold. Magnetic Resonance Imaging, 33, 639–647.Google Scholar
Ghaemi, M., Hilker, R., Rudolf, J., Sobesky, J., & Heiss, W.D. (2002). Differentiating multiple system atrophy from Parkinson's disease: Contribution of striatal and midbrain MRI volumetry and multi-tracer PET imaging. Journal of Neurology, Neurosurgery and Psychiatry, 73, 517–523.Google Scholar
Harrington, D.L., Haaland, K.Y., & Hermanowicz, N. (1998). Temporal processing in the basal ganglia. Neuropsychology, 12, 3–12.Google Scholar
Haslinger, B., Erhard, P., Kampfe, N., Boecker, H., Rummeny, E., Schwaiger, M., Conrad, B., & Ceballos-Baumann, A.O. (2001). Event-related functional magnetic resonance imaging in Parkinson's disease before and after levodopa. Brain, 124, 558–570.Google Scholar
Hoehn, M.M. & Yahr, M.D. (1967). Parkinsonism: Onset, progression, and mortality. Neurology, 17, 427–442.Google Scholar
Huettel, S.A., Singerman, J.D., & McCarthy, G. (2001). The effects of aging upon the hemodynamic response measured by functional MRI. Neuroimage, 13, 161–175.Google Scholar
Ivry, R.B. & Keele, S.W. (1989). Timing functions of the cerebellum. Journal of Cognitive Neuroscience, 1, 136–152.Google Scholar
Ivry, R.B., Keele, S.W., & Diener, H.C. (1988). Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Experimental Brain Research, 73, 167–180.Google Scholar
Jueptner, I.H., Flerich, L., Weiller, C., Mueller, S.P., & Diener, H.C. (1996). The human cerebellum and temporal information processing—Results from a PET experiment. NeuroReport, 7, 2761–2765.Google Scholar
Kaasinen, V. & Rinne, J.O. (2002). Functional imaging studies of dopamine system and cognition in normal aging and Parkinson's disease. Neuroscience and Biobehavioral Reviews, 26, 785–793.Google Scholar
Keele, S.W. & Ivry, R. (1990). Does the cerebellum provide a common computation for diverse tasks? A timing hypothesis. Annals of the New York Academy of Sciences, 608, 179–207.Google Scholar
Konczak, J., Ackermann, H., Hertrich, I., Speiker, S., & Dichgans, J. (1997). Control of repetitive lip and finger movements in Parkinson's disease: Influence of external timing signals and simultaneous execution on motor performance. Movement Disorders, 12, 665–676.Google Scholar
Meck, W.H. (1996). Neuropharmacology of timing and time perception. Cognitive Brain Research, 3, 227–242.Google Scholar
O'Boyle, D.J., Freeman, J.S., & Cody, F.W.J. (1996). The accuracy and precision of timing of self-paced, repetitive movements in subjects with Parkinson's disease. Brain, 119, 51–70.Google Scholar
Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97–113.Google Scholar
Pastor, M.A., Artieda, J., Jahanshahi, M., & Obeso, J.A. (1992a). Performance of repetitive wrist movements in Parkinson's disease. Brain, 115, 875–891.Google Scholar
Pastor, M.A., Artieda, J., Jahanshahi, M., & Obeso, J.A. (1992b). Time estimation and reproduction is abnormal in Parkinson's disease. Brain, 115, 211–225.Google Scholar
Penhune, V.B., Zatorre, R.J., & Evans, A. (1998). Cerebellar contributions to motor timing: A PET study of auditory and visual rhythm reproduction. Journal of Cognitive Neuroscience, 10, 752–765.Google Scholar
Picard, N. & Strick, P.L. (1996). Motor areas of the medial wall: A review of their location and functional activation. Cerebral Cortex, 6, 342–353.Google Scholar
Playford, E.D., Jenkins, I.H., Passingham, R.E., Frackowiak, R.S., & Brooks, D.J. (1993). Impaired activation of frontal areas during movement in Parkinson's disease: A PET study. Advances in Neurology, 60, 506–510.Google Scholar
Rao, S.M., Harrington, D.L., Haaland, K.Y., Bobholz, J.A., Cox, R.W., & Binder, J.R. (1997). Distributed neural systems underlying the timing of movements. Journal of Neuroscience, 17, 5528–5535.Google Scholar
Schmahmann, J.D., Doyon, J., Toga, A.W., Petrides, M., & Evans, A.C. (2000). MRI atlas of the human cerebellum. New York: Academic Press.
Sergent, V., Hellige, J.B., & Cherry, B. (1993). Effects of responding hand and concurrent verbal processing on time-keeping and motor-implementation processes. Brain and Cognition, 23, 243–262.Google Scholar
Talairach, J. & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme.
Thach, W.T. (1998a). A role for the cerebellum in learning movement coordination. Neurobiology of Learning and Memory, 70, 177–188.Google Scholar
Thach, W.T. (1998b). Combination, complementarity and automatic control: A role for the cerebellum in learning movement coordination. Novartis Foundation Symposium, 218, 219–228.Google Scholar
Thach, W.T., Goodkin, H.P., & Keating, J.G. (1992). The cerebellum and the adaptive coordination of movement. Annual Review of Neuroscience, 15, 403–442.Google Scholar
Thompson, P.M., Schwartz, C., Lin, R.T., Khan, A.A., & Toga, A.W. (1996). Three-dimensional statistical analysis of sucal variability in the human brain. Journal of Neuroscience, 16, 4261–4274.Google Scholar
Winer, B.J. (1971). Statistical principles in experimental design (2nd ed.). New York: McGraw-Hill.
Wing, A.M. & Kristofferson, A.B. (1973). Response delays and the timing of discrete motor responses. Perception and Psychophysics, 14, 5–12.Google Scholar