Experimental Brain Research

, Volume 161, Issue 3, pp 293–298 | Cite as

Memory-guided saccades in Parkinson’s disease: long delays can improve performance

  • Campbell J. Le Heron
  • Michael R. MacAskill
  • Tim J. Anderson
Research Article

Abstract

A recent study in control subjects suggested the existence of separate pathways for oculomotor spatial working memory tasks depending on whether the delay before movement execution is either short or long (>20 s). The long delay pathway might bypass brain areas commonly affected by Parkinson’s disease (PD). This study aimed to assess spatial working memory in Parkinson’s disease using short (3 s) and long (30 s) delays in a memory-guided saccade task. Fifteen mild-moderately affected PD subjects off-medication, and 15 age and sex-matched controls were tested (PD mean age 65.3; control 65.9). Subjects were tested in a darkened room using a horizontal LED bar to generate eye movements which were recorded using an infrared limbus tracker. Percentage error in amplitude of the primary saccade was analysed by repeated measures ANOVA. There was a significant interaction between the groups and their response to the short and long delay periods (P<0.02). PD subjects were more strongly impaired in the short delay than the long delay trials when compared with controls. Analysis of the percentage error in amplitude of the final eye position showed the same pattern but only in female subjects. This study provides the first evidence that the proposed parallel spatial memory pathway utilised in longer delay periods is relatively unimpaired in PD. In a broader sense, our results suggest there might be other alternative pathways to overcome deficits in functions impaired by PD.

Keywords

Parkinson’s disease Eye movement Memory-guided saccade Spatial working memory Dorsolateral prefrontal cortex 

References

  1. Bodis-Wollner I (2003) Neuropsychological and perceptual defects in Parkinson’s disease. Parkinsonism Relat Disord 9 Suppl 2: S83–89CrossRefGoogle Scholar
  2. Chafee MV, Goldman-Rakic PS (1998) Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. J Neurophysiol 79:2919–2940PubMedGoogle Scholar
  3. Chafee MV, Goldman-Rakic PS (2000) Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. J Neurophysiol 83:1550–1566PubMedGoogle Scholar
  4. Coffey CE, Lucke JF, Saxton JA, Ratcliff G, Unitas LJ, Billig B, Bryan RN (1998) Sex differences in brain aging: a quantitative magnetic resonance imaging study. Arch Neurol 55:169–179CrossRefPubMedGoogle Scholar
  5. Crawford TJ, Henderson L, Kennard C (1989) Abnormalities of nonvisually-guided eye movements in Parkinson’s disease. Brain 112:1573-1586PubMedGoogle Scholar
  6. Ding SL, Van Hoesen G, Rockland KS (2000) Inferior parietal lobule projections to the presubiculum and neighboring ventromedial temporal cortical areas. J Comp Neurol 425:510–530CrossRefPubMedGoogle Scholar
  7. Duff SJ, Hampson E (2001) A sex difference on a novel spatial working memory task in humans. Brain Cogn 47:470–493CrossRefPubMedGoogle Scholar
  8. Hodgson TL, Dittrich WH, Henderson L, Kennard C (1999) Eye movements and spatial working memory in Parkinson’s disease. Neuropsychologia 37:927–938CrossRefPubMedGoogle Scholar
  9. Kaasinen V, Nurmi E, Bruck A, Eskola O, Bergman J, Solin O, Rinne JO (2001) Increased frontal [18F]fluorodopa uptake in early Parkinson’s disease: sex differences in the prefrontal cortex. Brain 124:1125–1130CrossRefPubMedGoogle Scholar
  10. Ketcham CJ, Hodgson TL, Kennard C, Stelmach GE (2003) Memory-motor transformations are impaired in Parkinson’s disease. Exp Brain Res 149:30–39PubMedGoogle Scholar
  11. Kikuchi A, Takeda A, Kimpara T, Nakagawa M, Kawashima R, Sugiura M, Kinomura S, Fukuda H, Chida K, Okita N (2001) Hypoperfusion in the supplementary motor area, dorsolateral prefrontal cortex and insular cortex in Parkinson’s disease. Journal of the Neurological Sciences 193:29–36CrossRefPubMedGoogle Scholar
  12. Lavenex P, Suzuki WA, Amaral DG (2002) Perirhinal and parahippocampal cortices of the macaque monkey: projections to the neocortex. J Comp Neurol 447:394–420CrossRefPubMedGoogle Scholar
  13. Lueck CJ, Crawford TJ, Henderson L, Van Gisbergen JA, Duysens J, Kennard C (1992) Saccadic eye movements in Parkinson’s disease: II. Remembered saccades – towards a unified hypothesis? Q J Exp Psychol A 45:211–233PubMedGoogle Scholar
  14. Lueck CJ, Tanyeri S, Crawford TJ, Henderson L (1990) Antisaccades and remembered saccades in Parkinson’s disease. J Neurol Neurosurg Psychiatry 53:284–288PubMedGoogle Scholar
  15. MacAskill MR, Anderson TJ, Jones RD (2002) Adaptive modification of saccade amplitude in Parkinson’s disease. Brain 125:1570–1582CrossRefPubMedGoogle Scholar
  16. Muir SR, MacAskill MR, Herron D, Goelz H, Anderson TJ, Jones RD (2003) EMMA – an eye movement measurement and analysis system. Australasian Physical & Engineering Sciences in Medicine 26:18–24Google Scholar
  17. Müri RM, Gaymard B, Rivaud S, Vermersch A, Hess CW, Pierrot-Deseilligny C (2000) Hemispheric asymmetry in cortical control of memory-guided saccades. A transcranial magnetic stimulation study. Neuropsychologia 38:1105–1111CrossRefPubMedGoogle Scholar
  18. Müri RM, Vermersch AI, Rivaud S, Gaymard B, Pierrot-Deseilligny C (1996) Effects of single-pulse transcranial magnetic stimulation over the prefrontal and posterior parietal cortices during memory-guided saccades in humans. J Neurophysiol 76:2102–2106PubMedGoogle Scholar
  19. Nyffeler T, Pierrot-Deseilligny C, Felblinger J, Mosimann UP, Hess CW, Müri RM (2002) Time-dependent hierarchical organization of spatial working memory: a transcranial magnetic simulation study. Eur J Neurosci 16:1823–1827CrossRefPubMedGoogle Scholar
  20. Nyffeler T, Pierrot-Deseilligny C, Pflugshaupt T, Von Wartburg R, Hess CW, Müri RM (2004) Information processing in long delay memory-guided saccades: further insights from TMS. Exp Brain Res 154:109–112CrossRefPubMedGoogle Scholar
  21. O’Sullivan EP, Jenkins IH, Henderson L, Kennard C, Brooks DJ (1995) The functional anatomy of remembered saccades: a PET study. Neuroreport 6:2141–2144PubMedGoogle Scholar
  22. Pierrot-Deseilligny C, Müri RM, Ploner CJ, Gaymard B, Demeret S, Rivaud-Péchoux S (2002) Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour. Brain 126:1460–1473CrossRefGoogle Scholar
  23. Pierrot-Deseilligny C, Ploner CJ, Müri RM, Gaymard B, Rivaud-Péchoux S (2002) Effects of cortical lesions on saccadic eye movements in humans. Ann N Y Acad Sci 956:216–229PubMedGoogle Scholar
  24. Ploner CJ, Gaymard B, Rivaud S, Agid Y, Pierrot-Deseilligny C (1998) Temporal limits of spatial working memory in humans. Eur J Neurosci 10:794–797CrossRefPubMedGoogle Scholar
  25. Ploner CJ, Gaymard BM, Rivaud-Pechoux S, Baulac M, Clemenceau S, Samson S, Pierrot-Deseilligny C (2000) Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. Cereb Cortex 10:1211–1216CrossRefPubMedGoogle Scholar
  26. Reulen JPH, Marcus JT, Koops D, de Vries FR, Tiesinga G, Boshuizen K, Bos JE (1988) Precise recording of eye movement: the IRIS technique Part 1. Med Biol Eng Comput 26:20-26PubMedGoogle Scholar
  27. Selemon LD, Goldman-Rakic PS (1988) Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior. J Neurosci 8: 4049–4068PubMedGoogle Scholar
  28. Shaunak S, O’Sullivan E, Blunt S, Lawden M, Crawford T, Henderson L, Kennard C (1999) Remembered saccades with variable delay in Parkinson’s disease. Mov Disord 14:80–86CrossRefPubMedGoogle Scholar
  29. Sweeney JA, Mintun MA, Kwee S, Wiseman MB, Brown DL, Rosenberg DR, Carl JR (1996) Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J Neurophysiol 75:454–468PubMedGoogle Scholar
  30. Tsujimoto S, Sawaguchi T (2004) Properties of delay-period neuronal activity in the primate prefrontal cortex during memory- and sensory-guided saccade tasks. Eur J Neurosci 19:447–457CrossRefPubMedGoogle Scholar
  31. Yeterian EH, Pandya DN (1991) Prefrontostriatal connections in relation to cortical architectonic organization in rhesus monkeys. J Comp Neurol 312:43–67PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Campbell J. Le Heron
    • 1
  • Michael R. MacAskill
    • 1
    • 2
  • Tim J. Anderson
    • 1
    • 2
    • 3
  1. 1.Van der Veer Institute for Parkinson’s and Brain ResearchChristchurchNew Zealand
  2. 2.Department of Medicine, Christchurch School of Medicine and Health SciencesUniversity of OtagoChristchurchNew Zealand
  3. 3.Department of NeurologyChristchurch HospitalChristchurchNew Zealand

Personalised recommendations