Experimental Brain Research

, Volume 218, Issue 2, pp 295–304 | Cite as

Impaired savings despite intact initial learning of motor adaptation in Parkinson’s disease

  • Li-Ann Leow
  • Andrea M. Loftus
  • Geoffrey R. Hammond
Research Article

Abstract

In motor adaptation, the occurrence of savings (faster relearning of a previously learned motor adaptation task) has been explained in terms of operant reinforcement learning (Huang et al. in Neuron 70(4):787–801, 2011), which is thought to associate an adapted motor command with outcome success during repeated execution of the adapted movement. There is some evidence for deficient savings in Parkinson’s Disease (PD), which might result from deficient operant reinforcement processes. However, this evidence is compromised by limited adaptation training during initial learning and by multi-target adaptation, which reduces the number of reinforced movement repetitions for each target. Here, we examined savings in PD patients and controls following overlearning with a single target. PD patients showed less savings than controls after successive adaptation and deadaptation blocks within the same test session, as well as less savings across test sessions separated by a 24-h delay. It is argued that impaired blunted dopaminergic signals in PD impairs the modulation of dopaminergic signals to the motor cortex in response to rewarding motor outcomes, thus impairing the association of the adapted motor command with rewarding motor outcomes. Consequently, the previously adapted motor command is not preferentially selected during relearning, and savings is impaired.

Keywords

Savings Visuomotor adaptation Parkinson’s disease Motor learning 

Supplementary material

221_2012_3060_MOESM1_ESM.doc (934 kb)
Supplementary material 1 (DOC 934 kb)

References

  1. Bedard P, Sanes JN (2011) Basal ganglia-dependent processes in recalling learned visual-motor adaptations. Exp Brain Res 209:1–9CrossRefGoogle Scholar
  2. Brashers-Krug T, Shadmehr R, Bizzi E (1996) Consolidation in human motor memory. Nature 382(6588):252–255PubMedCrossRefGoogle Scholar
  3. Chaudhuri KR, Pal S, DiMarco A, Whately-Smith C, Bridgman K, Mathew R, Pezzela FR, Forbes A, Hogl B, Trenkwalder C (2002) The Parkinson’s disease sleep scale: a new instrument for assessing sleep and nocturnal disability in Parkinson’s disease. J Neurol Neurosurg Psychiatr 73(6):629–635PubMedCrossRefGoogle Scholar
  4. Cothros N, Kahler S, Dickie EW, Mirsattari SM, Gribble PL (2006) Proactive interference as a result of persisting neural representations of previously learned motor skills in primary motor cortex. J Cogn Neurosci 18(12):2167–2176. doi:10.1162/jocn.2006.18.12.2167 PubMedCrossRefGoogle Scholar
  5. Frank MJ (2005) Dynamic dopamine modulation in the basal ganglia: a neurocomputational account of cognitive deficits in medicated and nonmedicated Parkinsonism. J Cogn Neurosci 17(1):51–72PubMedCrossRefGoogle Scholar
  6. Frank MJ, Seeberger LC, O’Reilly RC (2004) By carrot or by stick: cognitive reinforcement learning in Parkinsonism. Science 306(5703):1940–1943PubMedCrossRefGoogle Scholar
  7. Galea JM, Vazquez A, Pasricha N, Orban de Xivry JJ, Celnik P (2010) Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cereb Cortex 23:34–35Google Scholar
  8. Goetz CG, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stebbins GT, Stern MB, Tilley BC, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, Van Hilten JJ, LaPelle N (2007) Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): Process, format, and clinimetric testing plan. Mov Disord 22(1):41–47PubMedCrossRefGoogle Scholar
  9. Huang V, Haith A, Mazzoni P, Krakauer J (2011) Rethinking motor learning and savings in adaptation paradigms: model-free memory for successful actions combines with internal models. Neuron 70(4):787–801PubMedCrossRefGoogle Scholar
  10. Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning. Nature 430(6995):78–81PubMedCrossRefGoogle Scholar
  11. Joiner WM, Smith MA (2008) Long-term retention explained by a model of short-term learning in the adaptive control of reaching. J Neurophysiol 100(5):2948–2955PubMedCrossRefGoogle Scholar
  12. Kapogiannis D, Mooshagian E, Campion P, Grafman J, Zimmermann TJ, Ladt KC, Wassermann EM (2011) Reward processing abnormalities in Parkinson’s disease. Mov Disord 26(8):1451–1457PubMedCrossRefGoogle Scholar
  13. Kish SJ, Shannak K, Hornykiewicz O (1988) Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson’s disease. N Engl J Med 318(14):876–880. doi:10.1056/NEJM198804073181402 PubMedCrossRefGoogle Scholar
  14. Krakauer JW, Pine ZM, Ghilardi MF, Ghez C (2000) Learning of visuomotor transformations for vectorial planning of reaching trajectories. J Neurosci 20(23):8916–8924PubMedGoogle Scholar
  15. Krakauer JW, Ghez C, Ghilardi MF (2005) Adaptation to visuomotor transformations: consolidation, interference, and forgetting. J Neurosci 25(2):473–478. doi:10.1523/jneurosci.4218-04.2005 PubMedCrossRefGoogle Scholar
  16. Landi SM, Baguear F, Della-Maggiore V (2011) One week of motor adaptation induces structural changes in primary motor cortex that predict long-term memory one year later. J Neurosci 31(33):11808–11813PubMedCrossRefGoogle Scholar
  17. Landsness EC, Crupi D, Hulse BK, Peterson MJ, Huber R, Ansari H, Coen M, Cirelli C, Benca RM, Ghilardi MF, Tononi G (2009) Sleep-dependent improvement in visuomotor learning: a causal role for slow waves. Sleep 32(10):1273–1284PubMedGoogle Scholar
  18. Li CSR, Padoa-Schioppa C, Bizzi E (2001) Neuronal correlates of motor performance and motor learning in the primary motor cortex of monkeys adapting to an external force field. Neuron 30(2):593–607PubMedCrossRefGoogle Scholar
  19. Luft AR, Schwarz S (2009) Dopaminergic signals in primary motor cortex. Int J Dev Neurosci 27(5):415–421PubMedCrossRefGoogle Scholar
  20. Marinelli L, Crupi D, Di Rocco A, Bove M, Eidelberg D, Abbruzzese G, Ghilardi MF (2009) Learning and consolidation of visuo-motor adaptation in Parkinson’s disease. Parkinsonism Relat D 15(1):6–11CrossRefGoogle Scholar
  21. Miall RC, Wolpert DM (1996) Forward models for physiological motor control. Neural Netw 9(8):1265–1279PubMedCrossRefGoogle Scholar
  22. Nasreddine ZS (2005) The Montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53(4):695PubMedCrossRefGoogle Scholar
  23. O’Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ (2004) Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304(5669):452–454PubMedCrossRefGoogle Scholar
  24. Orban de Xivry J-J, Criscimagna-Hemminger SE, Shadmehr R (2010) Contributions of the motor cortex to adaptive control of reaching depend on the perturbation schedule. Cereb Cortex. doi:10.1093/cercor/bhq192
  25. Pizzagalli DA, Evins AE, Schetter EC, Frank MJ, Pajtas PE, Santesso DL, Culhane M (2008) Single dose of a dopamine agonist impairs reinforcement learning in humans: behavioral evidence from a laboratory-based measure of reward responsiveness. Psychopharmacology 196(2):221–232PubMedCrossRefGoogle Scholar
  26. Richardson AG, Overduin SA, Valero-Cabre A, Padoa-Schioppa C, Pascual-Leone A, Bizzi E, Press DZ (2006) Disruption of primary motor cortex before learning impairs memory of movement dynamics. J Neurosci 26(48):12466–12470PubMedCrossRefGoogle Scholar
  27. Rutledge RB, Lazzaro SC, Lau B, Myers CE, Gluck MA, Glimcher PW (2009) Dopaminergic drugs modulate learning rates and perseveration in Parkinson’s patients in a dynamic foraging task. J Neurosci 29(48):15104–15114PubMedCrossRefGoogle Scholar
  28. Santesso DL, Evins AE, Frank MJ, Schetter EC, Bogdan R, Pizzagalli DA (2009) Single dose of a dopamine agonist impairs reinforcement learning in humans: evidence from event-related potentials and computational modeling of striatal-cortical function. Hum Brain Mapp 30(7):1963–1976PubMedCrossRefGoogle Scholar
  29. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80(1):1–27PubMedGoogle Scholar
  30. Seidler RD (2007) Aging affects motor learning but not savings at transfer of learning. Learn Mem 14(1–2):17PubMedCrossRefGoogle Scholar
  31. Shohamy D, Myers CE, Geghman KD, Sage J, Gluck MA (2006) L-dopa impairs learning, but spares generalization, Parkinson’s disease. Neuropsychologia 44(5):774–784PubMedCrossRefGoogle Scholar
  32. Smith MA, Ghazizadeh A, Shadmehr R (2006) Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol 4(6):1035–1043CrossRefGoogle Scholar
  33. Tanaka H, Sejnowski TJ, Krakauer JW (2009) Adaptation to visuomotor rotation through interaction between posterior parietal and motor cortical areas. J Neurophysiol 102(5):2921–2932PubMedCrossRefGoogle Scholar
  34. Thabit MN, Nakatsuka M, Koganemaru S, Fawi G, Fukuyama H, Mima T (2011) Momentary reward induce changes in excitability of primary motor cortex. Clin Neurophysiol 122(9):1764–1770PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Li-Ann Leow
    • 1
  • Andrea M. Loftus
    • 1
  • Geoffrey R. Hammond
    • 1
  1. 1.School of PsychologyThe University of Western AustraliaCrawleyAustralia

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