Abstract
Bradykinesia is one of the primary symptoms of Parkinson disease and leads to significant functional limitations for patients. Single joint movement studies, that have investigated the mechanism of bradykinesia, suggest that several features of muscle activity are disrupted, including modulation of burst amplitude and duration, and the number of bursts. It has been proposed that it is the blending of these different burst deficits that collectively defines bradykinesia. This study adds two new approaches to the study of bradykinesia. First, we examined the features of shoulder muscle activities during multijoint arm movement in bradykinetic and control subjects, such that previously reported single joint hypotheses could be tested for generalized arm movement. Second, we directly manipulated speed while keeping distance constant for a large range of speeds. In this manner, we could compare individual trials of muscle activity between controls and subjects with Parkinson’s disease (PD) for movements matched for both speed and movement duration. Our results showed that while a multiple burst pattern of shoulder muscles was a common strategy for all subjects (young, elderly controls and PD), subjects with PD showed several burst abnormalities, including deficits in initial agonist burst amplitude and duration at both fast and slow speeds. Subjects with PD also (1) failed to produce a one-burst pattern at fast speeds and, instead, produced a predominance of multiple burst patterns and (2) showed a relationship between the number of burst deficits and the severity of disease. These results extend the findings of single joint studies to multi-joint and similarly indicate that a combination of burst modulation abnormalities correlate with bradykinesia and disease severity.
Similar content being viewed by others
References
Alberts JL, Saling M, Adler CH, Stelmach GE (2000) Disruptions in the reach-to-grasp actions of Parkinson’s patients. Exp Brain Res 134:353–362
Almeida GK, Hong D, Corcos D, Gottlieb GL (1995) Organizing principles for voluntary movement: extending single-joint rules. J Neurophysiol 74:1374–1381
Awiszus F, Feistner H, Schafer SS (1991) On a method to detect long-latency excitations and inhibitions of single hand muscle motoneurons in man. Exp Brain Res 86:440–446
Baroni A, Benvenuti F, Fantini L, Pantaleo T, Urbani F (1984) Human ballistic arm abduction movements: effects of L-dopa treatment in Parkinson’s disease. Neurology 34:868–876
Benecke R, Rothwell JC, Dick JPR, Day BL, Marsden CD (1986) Performance of simultaneous movements in patients with Parkinson’s disease. Brain 109:739–757
Benecke R, Rothwell JC, Dick JPR, Day BL, Marsden CD (1987) Simple and complex movement off and on treatment in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 50:296–303
Berardelli A, Dick JPR, Rothwell JC, Day BL, Marsden CD (1986a) Scaling of the size of the first agonist EMG burst during rapid wrist movements in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 49:1273–1279
Berardelli A, Accornero N, Argenta M, Meco G, Manfredi M (1986b) Fast complex arm movements in Parkinson’s disease. J Neurol Neurosurg Psychiatry 49:1146–1149
Berardelli A, Hallett M, Rothwell JC, Agostino R, Manfredi M, Thompson PD, Marsden CD (1996) Single-joint rapid arm movements in normal subjects and in patients with motor disorders. Brain 119:661–674
Bond J, Morris M (2000) Goal-directed secondary motor tasks: their effects on gait in subjects with Parkinson’s disease. Arch Phys Med Rehabil 81:110–116
Brown SHC, Cooke JD (1981) Amplitude- and instruction-dependent modulation of movement-related electromyogram activity in humans. J Physiol 316:97–107
Brown RG, Marsden CD (1991) Dual task performance and processing resources in normal subjects and patients with Parkinson’s disease. Brain 114:215–231
Brown RG, Dowsey PL, Brown P, Jahanshahi M, Pollak P, Benabid AL, Rodriguez-Oroz MC, Obeso J, Rothwell JC (1999) Impact of deep brain stimulation on upper limb akinesia in Parkinson’s disease. Ann Neurol 45:473–488
Buneo C, Soechting JF, Flanders M (1994) Muscle activation patterns for reaching: the representation of distance and time. J Neurophysiol 71:1546–1558
Ellaway PH (1978) Cumulative sum technique and its application to the analysis of peristimulus time histograms. Clin Neurophysiol 45:302–304
Fahn S, Elton RL, Members of the UPDRS Development Committee (1987) Unified Parkinson’s Disease Rating Scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M et al. (eds) Recent developments in Parkinson’s disease, vol. 2. Macmillan Health Care Information, New York, pp 153–163
Flanders M, Herrmann U (1992) Two components of muscle activation: scaling with the speed of arm movement. J Neurophysiol 67:931–943
Galloway JC, Koshland GF (2001) General coordination of shoulder, elbow, wrist dynamics during multijoint arm movements. Exp Brain Res 142:163–180
Glas HW van der, Abbink JH, Bilt A van der, Cadden SW (1995) Analysis of differences between conditioned and control reflex series in EMG recordings. J Neurosci Methods 58:117–125
Godaux E, Koulischer D, Jacquy J (1992) Parkinsonian bradykinesia is due to depression in the rate of rise of muscle activity. Ann Neurol 31:93–100
Gottlieb GL, Corcos DM, Agarwal GC (1989) Strategies for the control of voluntary movements with one mechanical degree of freedom. Behav Brain Sci 12:189–250
Gottlieb GL, Chen CH, Corcos D (1996) Nonlinear control of movement distance at the human elbow. Exp Brain Res 112:289–297
Gottlieb GL, Song Q, Almeida GL, Hong D, Corcos D (1997) Directional control of planar human arm movements. J Neurophysiol 78:2985–2998
Gribble PL, Ostry DJ (1999) Compensation for interaction torques during single- and multijoint limb movement. J Neurophys 82:2310–2326
Hallett M, Khoshbin S (1980) A physiological mechanism of bradykinesia. Brain 103:301–314
Hallett M, Shahani BT, Young RR (1977) Analysis of stereotyped voluntary movements at the elbow in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 40:1129–1135
Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression, and mortality. Neurology 17:427–442
Hoffman DS, Strick PL (1990) Step-tracking movements of the wrist in humans. II. EMG analysis. J Neurosci 10:142–152
Hollerbach JM, Flash T (1982) Dynamic interactions between limb segments during planar arm movement. Biol Cybern 44:67–77
Kaminsky T, Gentile AM (1989) A kinematic comparison of single and multijoint pointing movements. Exp Brain Res 78:547–556
Ketcham CJ, Dounskaia N, Leis B, Stelmach GE (2000) Interactive torques contribute to multijoint coordination impairments in Parkinsonian patients. Soc Neurosci Abstr 26:62.11
Koshland GF, Marasli B, Arabyan A (1999) Directional effects of changes in muscle torques on initial path during simulated reaching movements. Exp Brain Res 128:353–368
Koshland GF, Galloway JC, Nevoret-Bell CJ (2000) Control of the wrist in three-joint arm movements to multiple directions in the horizontal plane. J Neurophysiol 83:3188–3195
Majsak MJ, Kaminski T, Gentile AM, Flanagan JR (1998) The reaching movements of patients with Parkinson’s disease under self-determined maximal speed and visually cued conditions. Brain 121:755–766
Morris ME, Iansek R, Matyas TA, Summers JJ (1994) The pathogenesis of gait hypokinesia in Parkinson’s disease. Brain 117:1161–1182
Mustard BE, Lee RG (1987) Relationship between EMG patterns and kinematic properties for flexion movements at the human wrist. Exp Brain Res 66:247–256
Pfann KD, Penn RD, Shannon KM, Corcos DM (1998) Pallidotomy and bradykinesia: implications for basal ganglia function. Neurology 51:796–803
Pfann KD, Buchman AS, Comella CL, Corcos DM (2001) Control of movement distance in Parkinson’s disease. Mov Disord 16:1048–1065
Phillips JG, Martin KE, Bradshaw JL, Iansek R (1994) Could bradykinesia in Parkinson’s disease simply be compensation? J Neurol 241:439–447
Poizner H, Feldman AG, Levin MF, Berkinblit MB, Hening WA, Patel A, Adamovich SV (2000) The timing of arm-trunk coordination is deficient and vision-dependent in Parkinson’s patients during reaching movements. Exp Brain Res 133:279–292
Rand MK, Van Gemmert AWA, Stelmach GE (2002) Segment difficulty in two-stroke movements in patients with Parkinson’s disease. Exp Brain Res 143:383–393
Schwab RS, Chafez ME, Walker S (1954) Control of two simultaneous voluntary motor acts in normals and in Parkinsonism. Arch Neurol Psychiatr 72:591–598
Seidler RD, Alberts JL, Stelmach GE (2001) Multijoint movement control in Parkinson’s disease. Exp Brain Res 140:335–344
Talland GA, Schwab RS (1964) Performance with multiple sets in Parkinson’s disease. Neuropsychologia 2:45–53
Teasdale N, Phillips J, Stelmach GE (1990) Temporal movement control in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 53:862–868
van den Berg C, Beek PJ, Wagenaar RC, van Wieringen PCW (2000) Coordination disorders in patients with Parkinson’s disease: a study of paced rhythmic forearm movements. Exp Brain Res 134:174–186
Wadman WJ, van der Gon DJJ, Derksen RJA (1980) Muscle activation patterns for fast goal directed arm movements. J Hum Mov Stud 6:19–27
Wierzbicka MM, Wiegner AW, Logigian EL, Young RR (1991) Abnormal most-rapid isometric contractions in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 54:210–216
Acknowledgements
This work was supported by NIH Training Grant NS07309. The authors thank Terrence Wyman and Greg Hockensmith for their extensive assistance during experiments and data analysis. We also wish to thank all of the elderly subjects and patients with Parkinson’s disease for volunteering their time to participate in this study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Farley, B.G., Sherman, S. & Koshland, G.F. Shoulder muscle activity in Parkinson’s disease during multijoint arm movements across a range of speeds. Exp Brain Res 154, 160–175 (2004). https://doi.org/10.1007/s00221-003-1654-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-003-1654-7