Experimental Brain Research

, Volume 179, Issue 2, pp 245–253 | Cite as

Perceptual factors contribute to akinesia in Parkinson’s disease

Research Article

Abstract

Parkinson’s disease (PD) patients have longer reaction time (RT) than age-matched control subjects. During the last decades, conflicting results have been reported regarding the source of this deficit. Here, we addressed the possibility that experimental inconsistencies originated in the composite nature of RT responses. To investigate this idea, we examined the effect of PD on different processes that compose RT responses. Three variables were manipulated: the signal quality, the stimulus–response compatibility and the foreperiod duration. These variables have been shown to affect, respectively, the ability to extract the relevant features of the stimulus (perceptual stage), the intentional selection of the motor response (cognitive stage) and the implementation of the muscle command (motor stage). Sixteen PD patients were tested on and off-medication and compared with an age and gender-matched control group. Results indicated that degrading the legibility of the response stimulus affected the latency of simple key-press movements more dramatically in the off-medication PD group than in the control population. The stimulus–response compatibility and the foreperiod duration had similar effects in the two groups. Interestingly, the response slowing associated with the degradation of the stimulus was the same whether the patients were on or off dopaminergic medication. This suggests that the high-level perceptual deficits observed in the present study do not have a dopaminergic origin.

Keywords

Parkinson’s disease Akinesia Choice reaction time Levodopa Perceptual slowing 

References

  1. Bachmann T, Asser T, Sarv M, Taba P, Lausvee E, Poder E, Kahusk N, Reitsnik T (1998) Speed of elementary visual recognition operations in Parkinson’s disease as measured by the mutual masking method. J Clin Exp Neuropsychol 20:118–134PubMedCrossRefGoogle Scholar
  2. Berardelli A, Rothwell JC, Thompson PD, Hallett M (2001) Pathophysiology of bradykinesia in Parkinson’s disease. Brain 124:2131–2146PubMedCrossRefGoogle Scholar
  3. Bertelson P (1967) The time course of preparation. Q J Exp Psychol 19:272–279PubMedGoogle Scholar
  4. Bonin-Guillaume S, Blin O, Hasbroucq T (2004) An additive factor analysis of the effect of depression on the reaction time of old patients. Acta Psychol 117:1–11CrossRefGoogle Scholar
  5. Broussolle E, Dentresangle C, Landais P, Garcia-Larrea L, Pollak P, Croisile B, Hibert O, Bonnefoi F, Galy G, Froment JC, Comar D (1999) The relation of putamen and caudate nucleus 18F-Dopa uptake to motor and cognitive performances in Parkinson’s disease. J Neurol Sci 166:141–151PubMedCrossRefGoogle Scholar
  6. Brown P, Marsden CD (1998) What do the basal ganglia do? Lancet 351:1801–1804PubMedCrossRefGoogle Scholar
  7. Courtiere A, Hardouin J, Vidal F, Possamai CA, Hasbroucq T (2003) An additive factor analysis of the effect of sub-anaesthetic doses of nitrous oxide on information processing: evidence for an impairment of the motor adjustment stage. Psychopharmacology 165:321–328PubMedGoogle Scholar
  8. Davranche K, Audiffren M (2002) Effects of a low dose of transdermal nicotine on information processing. Nicotine Tob Res 4:275–285PubMedCrossRefGoogle Scholar
  9. Davranche K, Audiffren M (2004) Facilitating effects of exercise on information processing. J Sports Sci 22:419–428PubMedCrossRefGoogle Scholar
  10. Deary IJ, Simonotto E, Meyer M, Marshall A, Marshall I, Goddard N, Wardlaw JM (2004) The functional anatomy of inspection time: an event-related fMRI study. Neuroimage 22:1466–1479PubMedCrossRefGoogle Scholar
  11. DeJong R, Liang C, Lauber E (1994) Conditional and unconditional automaticity: a dual-process model of effects of spatial stimulus–response correspondence. J Exp Psychol Hum Percept Perform 20:731–750CrossRefGoogle Scholar
  12. Desmurget M, Grafton ST, Vindras P, Grea H, Turner RS (2003) Basal ganglia network mediates the control of movement amplitude. Exp Brain Res 153:197–209PubMedCrossRefGoogle Scholar
  13. Desmurget M, Grafton ST, Vindras P, Grea H, Turner RS (2004) Basal ganglia network mediates the planning of movement amplitude. Eur J Neurosci 153:197–209Google Scholar
  14. Djamgoz MB, Hankins MW, Hirano J, Archer SN (1997) Neurobiology of retinal dopamine in relation to degenerative states of the tissue. Vis Res 37:3509–3529PubMedCrossRefGoogle Scholar
  15. Fielding J, Georgiou-Karistianis N, Bradshaw J, Millist L, White O (2005) No sequence dependent modulation of the Simon effect in Parkinson’s disease. Brain Res Cogn Brain Res 25:251–260PubMedCrossRefGoogle Scholar
  16. Fitts PM, Deininger RL (1954) S-R compatibility: correspondence among paired elements within stimulus and response codes. J Exp Psychol 48:483–492PubMedCrossRefGoogle Scholar
  17. Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198PubMedCrossRefGoogle Scholar
  18. Frith CD, Done DJ (1986) Routes to action in reaction time tasks. Psychol Res 48:169–177PubMedCrossRefGoogle Scholar
  19. Gauntlett-Gilbert J, Brown VJ (1998) Reaction time deficits and Parkinson’s disease. Neurosci Biobehav Rev 22:865–881PubMedCrossRefGoogle Scholar
  20. Godaux E, Koulischer D, Jacquy J (1992) Parkinsonian bradykinesia is due to depression in the rate of rise of muscle activity. Ann Neurol 31:93–100PubMedCrossRefGoogle Scholar
  21. Growdon JH, Kieburtz K, McDermott MP, Panisset M, Friedman JH (1998) Levodopa improves motor function without impairing cognition in mild non-demented Parkinson’s disease patients. Parkinson Study Group. Neurology 50:1327–1331PubMedGoogle Scholar
  22. Hasbroucq T, Mouret I, Seal J, Akamatsu M (1995) Finger pairings in two-choice reaction time tasks: does the between-hands advantage reflect response preparation? J Mot Behav 27:251–262PubMedCrossRefGoogle Scholar
  23. Hasbroucq T, Kaneko H, Akamatsu M, Possamai CA (1997) Preparatory inhibition of cortico-spinal excitability: a transcranial magnetic stimulation study in man. Brain Res Cogn Brain Res 5:185–192PubMedCrossRefGoogle Scholar
  24. Hasbroucq T, Osman A, Possamai CA, Burle B, Carron S, Depy D, Latour S, Mouret I (1999) Cortico-spinal inhibition reflects time but not event preparation: neural mechanisms of preparation dissociated by transcranial magnetic stimulation. Acta Psychol 101:243–266CrossRefGoogle Scholar
  25. Hasbroucq T, Tandonnet C, Micallef-Roll J, Blin O, Possamai CA (2003) An electromyographic analysis of the effect of levodopa on the response time of healthy subjects. Psychopharmacology 165:313–316PubMedGoogle Scholar
  26. Hayes AE, Davidson MC, Keele SW, Rafal RD (1998) Toward a functional analysis of the basal ganglia. J Cogn Neurosci 10:178–198PubMedCrossRefGoogle Scholar
  27. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442PubMedCrossRefGoogle Scholar
  28. Jackson S, Houghton G (1995) Sensorimotor selection and the basal ganglia: a neural network model. In: Houk J, Davis J, Beiser D (eds) Models of information processing in the basal ganglia. MIT Press, Cambridge, pp 337–368Google Scholar
  29. Jackson GR, Owsley C (2003) Visual dysfunction, neurodegenerative diseases, and aging. Neurol Clin 21:709–728PubMedCrossRefGoogle Scholar
  30. Jahanshahi M, Brown RG, Marsden CD (1992) The effect of withdrawal of dopaminergic medication on simple and choice reaction time and the use of advance information in Parkinson’s disease. J Neurol Neurosurg Psychiatr 55:1168–1176PubMedCrossRefGoogle Scholar
  31. Jenkins IH, Fernandez W, Playford ED, Lees AJ, Frackowiak RS, Passingham RE, Brooks DJ (1992) Impaired activation of the supplementary motor area in Parkinson’s disease is reversed when akinesia is treated with apomorphine. Ann Neurol 32:749–757PubMedCrossRefGoogle Scholar
  32. Johnson AM, Almeida QJ, Stough C, Thompson JC, Singarayer R, Jog MS (2004) Visual inspection time in Parkinson’s disease: deficits in early stages of cognitive processing. Neuropsychologia 42:577–583PubMedCrossRefGoogle Scholar
  33. Kornblum S, Hasbroucq T, Osman A (1990) Dimensional overlap: cognitive basis for stimulus–response compatibility. A model and taxonomy. Psychol Rev 97:253–270PubMedCrossRefGoogle Scholar
  34. Kropotov JD, Etlinger SC (1999) Selection of actions in the basal ganglia-thalamocortical circuits: review and model. Int J Psychophysiol 31:197–217PubMedCrossRefGoogle Scholar
  35. Labyt E, Devos D, Bourriez JL, Cassim F, Destee A, Guieu JD, Defebvre L, Derambure P (2003) Motor preparation is more impaired in Parkinson’s disease when sensorimotor integration is involved. Clin Neurophysiol 114:2423–2433PubMedCrossRefGoogle Scholar
  36. Lennie P (1998) Single units and visual cortical organization. Perception 27:889–935PubMedCrossRefGoogle Scholar
  37. Low KA, Miller J, Vierck E (2002) Response slowing in Parkinson’s disease: a psychophysiological analysis of premotor and motor processes. Brain 125:1980–1994PubMedCrossRefGoogle Scholar
  38. Mann DM, Yates PO (1983) Pathological basis for neurotransmitter changes in Parkinson’s disease. Neuropathol Appl Neurobiol 9:3–19PubMedGoogle Scholar
  39. Marien MR, Colpaert FC, Rosenquist AC (2004) Noradrenergic mechanisms in neurodegenerative diseases: a theory. Brain Res Brain Res Rev 45:38–78PubMedCrossRefGoogle Scholar
  40. Marx M, Bodis-Wollner I, Bodak P, Harnois C, Mylin L, Yahr M (1986) Temporal frequency-dependent VEP changes in Parkinson’s disease. Vision Res 26:185–193PubMedCrossRefGoogle Scholar
  41. Nissen MJ (1977) Stimulus intensity and information processing. Percept Psychophysiol 22:338–352Google Scholar
  42. Pillon B, Dubois B, Bonnet AM, Esteguy M, Guimaraes J, Vigouret JM, Lhermitte F, Agid Y (1989) Cognitive slowing in Parkinson’s disease fails to respond to levodopa treatment: the 15–objects test. Neurology 39:762–768PubMedGoogle Scholar
  43. Playford ED, Jenkins IH, Passingham RE, Nutt J, Frackowiak RS, Brooks DJ (1992) Impaired mesial frontal and putamen activation in Parkinson’s disease: a positron emission tomography study. Ann Neurol 32:151–161PubMedCrossRefGoogle Scholar
  44. Praamstra P, Plat FM (2001) Failed suppression of direct visuomotor activation in Parkinson’s disease. J Cogn Neurosci 13:31–43PubMedCrossRefGoogle Scholar
  45. Praamstra P, Stegeman DF, Cools AR, Horstink MW (1998) Reliance on external cues for movement initiation in Parkinson’s disease. Evidence from movement-related potentials. Brain 121:167–177PubMedCrossRefGoogle Scholar
  46. Praamstra P, Plat EM, Meyer AS, Horstink MW (1999) Motor cortex activation in Parkinson’s disease: dissociation of electrocortical and peripheral measures of response generation. Mov Disord 14:790–799PubMedCrossRefGoogle Scholar
  47. Rafal RD, Posner MI, Walker JA, Friedrich FJ (1984) Cognition and the basal ganglia. Separating mental and motor components of performance in Parkinson’s disease. Brain 107:1083–1094PubMedCrossRefGoogle Scholar
  48. Redgrave P, Prescott TJ, Gurney K (1999) The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89:1009–1023PubMedCrossRefGoogle Scholar
  49. Reeve TG, Proctor RW (1990) The salient features coding principle for spatial- and symbolic-compatibility effects. In: Proctor RW, Reeve TG (eds) Stimulus–response compatibility: an integrated perspective. Adv Psychol, vol 65. North-Holland, Amsterdam, pp 163–180Google Scholar
  50. Ridderinkhof KR, van der Molen MW (1995) When global information and local information collide: a brain potential analysis of the locus of interference effects. Biol Psychol 41: 29–53PubMedCrossRefGoogle Scholar
  51. Rihet P, Possamai CA, Micallef-Roll J, Blin O, Hasbroucq T (2002) Dopamine and human information processing: a reaction-time analysis of the effect of levodopa in healthy subjects. Psychopharmacology 163:62–67PubMedCrossRefGoogle Scholar
  52. Robbins TW (1997) Arousal systems and attentional processes. Biol Psychol 45:57–71PubMedCrossRefGoogle Scholar
  53. Robbins TW, Brown VJ (1990) The role of the striatum in the mental chronometry of action: a theoretical review. Rev Neurosci 2:181–213Google Scholar
  54. Sanders AF (1980) Stage analysis of reaction processes. In: Stelmach GE, Requin J (eds) Tutorials in motor behaviour. North-Holland, Amsterdam, pp 331–354Google Scholar
  55. Sanders AF (1983) Towards a model of stress and human performance. Acta Psychol 53:61–97CrossRefGoogle Scholar
  56. Sanders AF (1998) Elements of human performance: reaction processes and attention in human skills. Laurence Erlbaum, MahwahGoogle Scholar
  57. Shipley BA, Deary IJ, Tan J, Christie G, Starr JM (2002) Efficiency of temporal order discrimination as an indicator of bradyphrenia in Parkinson’s disease: the inspection time loop task. Neuropsychologia 40:1488–1493PubMedCrossRefGoogle Scholar
  58. Spijkers WAC, Walter A (1985) Response processing stages in choice reactions. Acta Psychol 58:191–204CrossRefGoogle Scholar
  59. Sternberg S (1969) The discovery of processing stages: extensions of Donders’ method. Acta Psychol 30:276–315CrossRefGoogle Scholar
  60. Sternberg S (2001) Separate modifiability, mental modules, and the use of pure and composite measures to reveal them. Acta Psychol 106:147–246CrossRefGoogle Scholar
  61. Tandonnet C, Burle B, Vidal F, Hasbroucq T (2003) The influence of time preparation on motor processes assessed by surface Laplacian estimation. Clin Neurophysiol 114:2376–2384PubMedCrossRefGoogle Scholar
  62. Turner RS, Desmurget M, Grethe J, Crutcher MD, Grafton ST (2003) Motor subcircuits mediating the control of movement extent and speed. J Neurophysiol 90:3958–3966PubMedCrossRefGoogle Scholar
  63. Van Der Molen MW, Bashore TR, Halliday R, Callaway E (1991) Chronopsychophysiology: mental chronometry augmented with physiological measures. In: Jennings JR, Coles MGH (eds) Handbook of cognitive psychophysiology, Wiley, Chichester, pp 9–178Google Scholar
  64. Werheid K, Ziessler M, Nattkemper D, von Cramon DY (2003) Sequence learning in Parkinson’s disease: the effect of spatial stimulus–response compatibility. Brain Cogn 52:239–249PubMedCrossRefGoogle Scholar
  65. Winer BJ (1971) Statistical principles in experimental design. McGraw Hill, LondonGoogle Scholar
  66. Wylie SA, Stout JC, Bashore TR (2005) Activation of conflicting responses in Parkinson’s disease: evidence for degrading and facilitating effects on response time. Neuropsychologia 43:1033–1043PubMedCrossRefGoogle Scholar
  67. Zhang HH, Zhang J, Kornblum S (1999) A parallel distributed processing model of stimulus-stimulus and stimulus–response compatibility. Cognit Psychol 38:386–432PubMedCrossRefGoogle Scholar
  68. Zimmermann P, Sprengelmeyer R, Fimm B, Wallesch CW (1992) Cognitive slowing in decision tasks in early and advanced Parkinson’s disease. Brain Cogn 18:60–69PubMedCrossRefGoogle Scholar
  69. Zorzi M, Umilta C (1995) A computational model of the Simon effect. Psychol Res 58:193–205PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • B. Ballanger
    • 1
    • 2
    • 3
  • R. Gil
    • 2
  • M. Audiffren
    • 1
  • M. Desmurget
    • 3
  1. 1.Laboratoire Performance Motricité et CognitionUniversity of PoitiersPoitiersFrance
  2. 2.Neurology DepartmentPoitiers University HospitalPoitiersFrance
  3. 3.INSERM, U 371, Brain and Vision ResearchBronFrance

Personalised recommendations