Skip to main content
SpringerLink
Log in

Memory-motor transformations are impaired in Parkinson's disease

Experimental Brain Research volume 149, pages 30–39 (2003)Cite this article

Abstract

Parkinson's disease patients are known to suffer loss of dopaminergic input to the rostral caudate nucleus. Recent functional magnetic resonance imaging (fMRI) studies have implicated this structure in the transformation of spatial information in memory to guide action, suggesting that memory to motor transformations may be selectively impaired in Parkinson's disease. In order to investigate this possibility we tested a group of Parkinson's disease patients (PDs) using a memory-guided pointing task. Of interest was whether patients showed reduced accuracy in the task as a function of memory load. Twelve PD patients and 13 elderly controls were asked to recall single or four step target sequences with 2 time delays (500 and 3,500 ms). In all memory-guided conditions PD patients showed increased variability in memory-guided movement end-points. This effect was not affected by delay, number of items, or the sequence familiarity. The results are consistent with increased variability in memory-motor transformations in early PD, due to dopamine depletion within the rostral caudate nucleus.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1.
Fig. 2.
Fig. 3. a

Notes

  1. This also enhances the ecological validity of our study as no constraints are put on eye movements in standard clinical assessment of spatial memory functions.

References

  • Alberts JL, Tresilian JR, Stelmach GE (1998) Coordination and phasing of a bilateral prehension task: the influence of Parkinson's disease. Brain 121:725–742

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Baddeley A, Della Sala S (1996) Working memory and executive control. Philos Trans R Soc Lond B 351:1397–1404

    CAS  PubMed  Google Scholar 

  • Bekkering H, Neggers SFW, Walker R, Gleibner B, Dittrich WH, Kennard C (2001) The preparation and execution of saccadic eye and goal-directed hand movements in patients with Parkinson's disease. Neuropsychologia 39:173–183

    Article  CAS  PubMed  Google Scholar 

  • Berry EL, Nicolson RI, Foster JK, Behrmann M, Sagar HJ (1999) Slowing of reaction time in Parkinson['s disease]: the involvement of the frontal lobes. Neuropsychologia 37:787–795

    CAS  PubMed  Google Scholar 

  • Bradley VA, Welsh JL, Dick DJ (1989) Visuo-spatial working memory in Parkinson's disease. J Neurol Neurosurg Psychiatry 52:1228–1235

    CAS  PubMed  Google Scholar 

  • Briand KA, Strallow D, Hening W, Poizner H, Sereno AB (1999) Control of voluntary and reflexive saccades in Parkinson's disease. Exp Brain Res 129:38–48

    Article  CAS  PubMed  Google Scholar 

  • Brown RG, Marsden CD (1988) Internal versus external cues and the control of attention in Parkinson's disease. Brain 111:323–345

    PubMed  Google Scholar 

  • Brown RG, Marsden CD (1990) Cognitive function in Parkinson's disease: from description to theory. Trends Neurosci 13:21–28

    CAS  PubMed  Google Scholar 

  • Calne DB (2001) Parkinson's disease is not one disease. Parkinsonism Related Disord 7:3–7

    Article  Google Scholar 

  • Clark A (1997) Being there: putting brain, body and world together again. MIT Press, Massachusetts

    Google Scholar 

  • Cooper JA, Sagar HJ, Jordan N, Harvey NS, Sullivan EV (1991) Cognitive impairment in early, untreated Parkinson's disease and its relationship to motor disability. Brain 114:2095–2122

    PubMed  Google Scholar 

  • Crawford TJ, Henderson L, Kennard C (1989) Abnormalities of non-visual guided eye movements in Parkinson's disease. Brain 112:1573–1586

    PubMed  Google Scholar 

  • Demirci M, Grill S, McShane L, Hallet M (1997) A mismatch between kinesthetic and visual perception in Parkinson's disease. Ann Neurol 41:781–788

    CAS  PubMed  Google Scholar 

  • Dujardin K, Defebvre L, Grunberg C, Becquet E, Destee A (2001) Memory and executive function in sporadic and familial Parkinson's disease. Brain 124:389–398

    Article  CAS  PubMed  Google Scholar 

  • Fahn S, Elton RL, Members of the UPDRS Development Committee (1987) Unified Parkinson's Disease Rating Scale. In: Fahn S, Marsden CD, Goldstein M, Calne DB (eds) Recent developments in Parkinson's disease, vol 2. Macmillan, New York, pp 153–163

  • Fischer MH (2001) Probing spatial working memory with the Corsi Blocks task. Brain Cogn 45:143–154

    Article  CAS  PubMed  Google Scholar 

  • Flowers KA, Pearce I, Pearce JMS (1984) Recognition memory in Parkinson's disease. J Neurol Neurosurg Psychiatry 47:1174–1181

    CAS  PubMed  Google Scholar 

  • Folstein MF, Folstein SE, McHugh PR (1975) "Mini mental state": a practical method for grading the cognitive state of patients of the clinician. J Psychiatr Res 12:189–198

    CAS  PubMed  Google Scholar 

  • Fournet N, Moreaud O, Naegele B, Pellat J (1996) Working memory in medicated patients with Parkinson's disease: the central executive seems to work. J Neurol Neurosurg Psychiatry 60:313–317

    CAS  PubMed  Google Scholar 

  • Giraudo M-D, Gayraud D, Habib M (1997) Visuospatial ability of Parkinsonians and elderly adults in location memory tasks. Brain Cogn 34:259–273

    Article  CAS  PubMed  Google Scholar 

  • Gotham AM, Brown RG, Marsden CD (1988) Frontal cognitive function in patients with Parkinson's disease on and off levodopa. Brain 111:299–321

    PubMed  Google Scholar 

  • Harrison JE, Stow I, Owen AM (2002) Parkinson's disease. In: Harrison JE, Owen AM (eds) Cognitive and brain disorders. Martin Dunitz, London, pp 197–216

  • Henderson L, Harrison J, Kennard C (2001) Selectively impaired reaction time in Parkinson's disease: persistent absence of simple reaction advantage in a patient with frontal complications. Neurocase 7:319–330

    Article  CAS  PubMed  Google Scholar 

  • Hodgson TL, Dittrich W, Henderson L, Kennard C (1999) Eye movements and spatial working memory in Parkinson's disease. Neuropsychologia 37:927–938

    Article  CAS  PubMed  Google Scholar 

  • Hodgson TL, Bajwa A, Owen AM, Kennard C (2000) Strategic control of gaze direction during the Tower of London task. J Cogn Neurosci 12:894–907

    Article  CAS  PubMed  Google Scholar 

  • Hodgson TL, Tiesman B, Owen AM, Kennard C (2002) Abnormal gaze strategies during problem solving in Parkinson's disease. Neuropsychologia 40:411–422

    Article  CAS  PubMed  Google Scholar 

  • Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:749–757

    Google Scholar 

  • Ivory S-J, Knight RG, Longmore BE, Caradoc-Davies T (1999) Verbal memory in non-demented patients with idiopathic Parkinson's disease. Neuropsychologia 37:817–828

    Article  CAS  PubMed  Google Scholar 

  • Ketcham CJ, Hodgson TL, Kennard C, Stelmach GE (2001) Spatial working memory is selectively impaired in early Parkinson's disease. J Cogn Neurosci (Suppl):86

    Google Scholar 

  • Kirsh D, Maglio P (1994) On distinguishing between epistemic and pragmatic action. Cogn Sci 18:513–549

    Article  Google Scholar 

  • Kish SJ, Shannak K, Hornykiewicz O (1988) Uneven patterns of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N Engl J Med 318:876–880

    CAS  PubMed  Google Scholar 

  • Lee AC, Harris JP, Calvert JE (1998) Impairments of mental rotation in Parkinson's disease. Neuropsychologia 36:109–114

    Article  CAS  PubMed  Google Scholar 

  • Levy R, Friedman HR, Davachi L, Goldman-Rakic PS (1997) Differential activation of the caudate nucleus in primates performing spatial and nonspatial working memory tasks. J Neurosci 17:3870–3882

    CAS  PubMed  Google Scholar 

  • Lueck CJ, Tanyeri S, Crawford TJ, Henderson L, Kennard C (1990) Antisaccades and remembered saccades in Parkinson's disease. J Neurol Neurosurg Psychiatry 53:284–288

    CAS  PubMed  Google Scholar 

  • Lueck CJ, Crawford TL, Henderson L, Van Gisbergen JAM, Duysens J (1992) Saccadic eye movements in Parkinson's disease: II Remembered saccades—towards a unified hypothesis? Q J Exp Psychol 45A:211–233

    Google Scholar 

  • Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev 31:236–250

    Article  CAS  PubMed  Google Scholar 

  • Nurmi E, Ruottinen HM, Bergman J, Haaparanta M, Solin O, Sonninen P, Rinne JO (2001) Rate of progression in Parkinson's disease: a 6-[18F]fluoro-l-dopa PET study. Mov Disord 16:608–615

    Article  CAS  PubMed  Google Scholar 

  • Owen AM, James M, Leigh PN, Summers BA, Marsden CD, Quinn NP, Lange KW, Robbins TW (1992) Fronto-striatal cognitive deficits at different stages of Parkinson's disease. Brain 115:1727–1751

    PubMed  Google Scholar 

  • Owen AM, Iddon JL, Hodge JR, Summers BA, Robbins TW (1997) Spatial and non-spatial working memory at different stages of Parkinson's disease. Neuropsychologia 35:519–532

    Article  CAS  PubMed  Google Scholar 

  • Postle BR, D'Esposito M (1999) Dissociation of human caudate nucleus activity in spatial and nonspatial working memory: an event-related fMRI study. Cogn Brain Res 8:107–115

    CAS  Google Scholar 

  • Praamstra P, Stegeman DF, Cools AR, Horstink MWIM (1998) Reliance on external cues for movement initiation in Parkinson's disease: evidence from movement-related potentials. Brain 121:167–177

    Article  PubMed  Google Scholar 

  • Rafal RD, Posner MI, Walker JA, Friedrich FJ (1984) Cognition and the basal ganglia. Brain 107:1083–1094

    PubMed  Google Scholar 

  • Rakshi JS, Uema T, Ito K, Bailey DL, Morrish PK, Ashburner J, Dagher A, Jenkins IH, Friston KJ, Brooks DJ (1999) Frontal, midbrain and striatal dopaminergic function in early and advanced Parkinson's disease: a 3D [18F]dopa-PET study. Brain 122:1637–1650

    Article  PubMed  Google Scholar 

  • Rand MK, Stelmach GE (2000) Movement accuracy constraints in Parkinson's disease patients. Exp Brain Res 38:203–212

    Article  CAS  Google Scholar 

  • Russ MO, Seger L (1995) The effect of task complexity on reaction times in memory scanning and visual discrimination in Parkinson's disease. Neuropsychologia 33:561–575

    Article  CAS  PubMed  Google Scholar 

  • Shallice T, Burgess PW (1996) The domain of supervisory processes and temporal organization of behaviour. Philos Trans R Soc Lond B 351:1405–1412

    CAS  Google Scholar 

  • Stebbins GT, Gabrieli JDE, Masciari F, Monti L, Goetz CG (1999) Delayed recognition memory in Parkinson's disease: a role for working memory? Neuropsychology 37:503–510

    Article  CAS  Google Scholar 

  • Swinnen SP, Steyvers M, VanDenBergh L, Stelmach GE (2000) Motor learning and Parkinson's disease: refinement of within-limb and between-limb coordination as a result of practice. Behav Brain Res 111:45–49

    Article  CAS  PubMed  Google Scholar 

  • Teulings HL, Contreras-Vidal J, Stelmach GE (1997) Coordination of fingers, wrist, and arm in Parkinsonian handwriting. Exp Neurol 146:159–170

    CAS  PubMed  Google Scholar 

  • Van Spaendonck KPM, Berger HJC, Horstink MWIM, Borm GH, Cools AR (1996) Memory performance under varying cueing conditions in patients with Parkinson's disease. Neuropsychologia 34:1159–1164

    Article  PubMed  Google Scholar 

  • Vermasch A, Rivaud S, Vidailhet M, Bonner A, Gaymard B, Agid Y, Pierrot-Deseilligny C (1994) Sequences of memory guided saccades in Parkinson's disease. Ann Neurol 35:487–490

    PubMed  Google Scholar 

  • Webster DD (1968) Critical analysis of the disability in Parkinson's disease. Mod Treatment 5:257–282

    CAS  Google Scholar 

  • Wilson RS, Kaszniak AW, Klawans HL, Garron DC (1980) High speed memory scanning in Parkinsonism. Cortex 16:67–71

    CAS  PubMed  Google Scholar 

  • Wolpert D, Ghahramani Z, Jordan MI (1995) An internal model for sensory motor integration. Science 269:1880–1882

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements.

This work was supported by NS 43502 and NS 39352 Grants from the National Institute of Neurological Diseases and Strokes as well as a Burroughs-Wellcome Award awarded to George E. Stelmach. A portion of this research was presented at the 2001 Cognitive Neuroscience Conference in New York.

Author information

Authors and Affiliations

  1. Motor Control Laboratory, Arizona State University, PO Box 870404, Tempe, AZ , 85287-0404, USA

    Caroline J. Ketcham & George E. Stelmach

  2. School of Psychology, University of Exeter, Exeter , EX4 4QG, UK

    Timothy L. Hodgson

  3. Division of Neuroscience, Imperial College, Charing Cross Campus, London, UK

    Christopher Kennard

Authors
  1. Caroline J. Ketcham
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Timothy L. Hodgson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher Kennard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. George E. Stelmach
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to George E. Stelmach.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Ketcham, C.J., Hodgson, T.L., Kennard, C. et al. Memory-motor transformations are impaired in Parkinson's disease. Exp Brain Res 149, 30–39 (2003). https://doi.org/10.1007/s00221-002-1332-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-002-1332-1

Keywords

search

Navigation