Skip to main content

Advertisement

Log in

What neurological diseases tell us about procedural perceptual-motor learning? A systematic review of the literature

  • Review Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Introduction

Procedural perceptual-motor learning of sequences (PPMLS) provides perceptual-motor skills in many activities of daily living. Based on behavioral and neuroimaging results, theoretical models of PPMLS postulate that the cortico-striatal loop, the cortico-cerebellar loop and the hippocampus are specifically involved in the early stage of PPMLS while the cortico-striatal loop would be specifically involved in the late stage of PPMLS. Hence, current models predict that the early stage of PPMLS should be impaired in Parkinson’s disease (PD: lesion of the cortico-striatal loop), in cerebellar disease (CD: lesion of the cortico-cerebellar loop) and in Alzheimer’s disease (AD: lesion of the hippocampus), whereas the late stage of PPMLS should be specifically impaired in PD.

Objective

The aim of the study is (1) to draw a complete picture of experimental results on PPMLS in PD, CD and AD (2) to understand heterogeneity of results as regard to participant and task characteristics.

Method

This review is based on the guideline proposed by the PRISMA statement.

Results

Our review reveals (1) that the experimental results clarify the theoretical models and (2) that the impairment of PPMLS depends on both the personal characteristics of the participants and the characteristics of the task to-be-learnt rather than on the disease itself.

Conclusion

Our results highlight that these characteristics should be more carefully considered to understand the heterogeneity of results across studies on PPMLS and the effects of rehabilitation programs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Eustache F, Viard A, Desgranges B (2016) The MNESIS model: memory systems and processes, identity and future thinking. Neuropsychologia 87:96–109. https://doi.org/10.1016/j.neuropsychologia.2016.05.006

    Article  PubMed  Google Scholar 

  2. Squire LR, Zola SM (1996) Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci 93(24):13515–13522. https://doi.org/10.1073/pnas.93.24.13515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Milner B, Corkin S, Teuber H-L (1968) Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M. Neuropsychologia 6(3):215–234. https://doi.org/10.1016/0028-3932(68)90021-3

    Article  Google Scholar 

  4. Tulving E, Markowitsch HJ (1998) Episodic and declarative memory: role of the hippocampus. Hippocampus 8(3):198–204

    Article  CAS  PubMed  Google Scholar 

  5. Doyon J, Laforce R, Bouchard G, Gaudreau D, Roy J, Poirier M, Bouchard J-P (1998) Role of the striatum, cerebellum and frontal lobes in the automatization of a repeated visuomotor sequence of movements. Neuropsychologia 36(7):625–641. https://doi.org/10.1016/S0028-3932(97)00168-1

    Article  CAS  PubMed  Google Scholar 

  6. Cohen N, Squire L (1980) Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. Science 210(4466):207–210. https://doi.org/10.1126/science.7414331

    Article  CAS  PubMed  Google Scholar 

  7. Janacsek K, Nemeth D (2012) Predicting the future: from implicit learning to consolidation. Int J Psychophysiol 83(2):213–221. https://doi.org/10.1016/j.ijpsycho.2011.11.012

    Article  PubMed  Google Scholar 

  8. Reber PJ, Squire LR (1994) Parallel brain systems for learning with and without awareness. Learn Mem 1(4):217–229

    Article  CAS  PubMed  Google Scholar 

  9. Doyon J, Penhune V, Ungerleider LG (2003) Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41(3):252–262. https://doi.org/10.1016/S0028-3932(02)00158-6

    Article  PubMed  Google Scholar 

  10. Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams MM, Turner R, Ungerleider LG (1998) The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci 95(3):861–868. https://doi.org/10.1073/pnas.95.3.861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Karni A (1996) The acquisition of perceptual and motor skills: a memory system in the adult human cortex. Cogn Brain Res 5(1–2):39–48. https://doi.org/10.1016/S0926-6410(96)00039-0

    Article  CAS  Google Scholar 

  12. Ammons RB, Farr RG, Bloch E, Neumann E, Dey M, Marion R, Ammons CH (1958) Long-term retention of perceptual-motor skills. J Exp Psychol 55(4):318–328. https://doi.org/10.1037/h0041893

    Article  CAS  PubMed  Google Scholar 

  13. Neumann E, Ammons RB (1957) Acquisition and long-term retention of a simple serial perceptual-motor skill. J Exp Psychol 53(3):159–161. https://doi.org/10.1037/h0041719

    Article  CAS  PubMed  Google Scholar 

  14. Fleishman EA, Parker JF Jr (1962) Factors in the retention and relearning of perceptual-motor skill. J Exp Psychol 64(3):215–226. https://doi.org/10.1037/h0041220

    Article  CAS  PubMed  Google Scholar 

  15. Brown RM, Robertson EM, Press DZ (2009) Sequence skill acquisition and off-line learning in normal aging. PLoS ONE 4(8):e6683. https://doi.org/10.1371/journal.pone.0006683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Howard DV, Howard JH (1989) Age differences in learning serial patterns: Direct versus indirect measures. Psychol Aging 4(3):357–364. https://doi.org/10.1037/0882-7974.4.3.357

    Article  CAS  PubMed  Google Scholar 

  17. Desgranges B (1998) The neural substrates of memory systems impairment in Alzheimer’s disease. A PET study of resting brain glucose utilization. Brain 121(4):611–631. https://doi.org/10.1093/brain/121.4.611

    Article  PubMed  Google Scholar 

  18. Desgranges B, Eustache F (2011) Les conceptions de la mémoire déclarative d’Endel Tulving et leurs conséquences actuelles. Rev Neuropsychol 3(2):94. https://doi.org/10.3917/rne.032.0094

    Article  Google Scholar 

  19. Cavaco S (2004) The scope of preserved procedural memory in amnesia. Brain 127(8):1853–1867. https://doi.org/10.1093/brain/awh208

    Article  PubMed  Google Scholar 

  20. Nissen MJ, Bullemer P (1987) Attentional requirements of learning: evidence from performance measures. Cogn Psychol 19(1):1–32. https://doi.org/10.1016/0010-0285(87)90002-8

    Article  Google Scholar 

  21. Robertson EM (2007) The serial reaction time task: implicit motor skill learning? J Neurosci 27(38):10073–10075. https://doi.org/10.1523/JNEUROSCI.2747-07.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Romano JC, Howard JH, Howard DV (2010) One-year retention of general and sequence-specific skills in a probabilistic, serial reaction time task. Memory 18(4):427–441. https://doi.org/10.1080/09658211003742680

    Article  PubMed  PubMed Central  Google Scholar 

  23. Doyon J, and Benali H (2005) Reorganization and plasticity in the adult brain during learning of motor skills. In Proceedings. 2005 IEEE International Joint Conference on Neural Networks, 2005. (Vol 3, pp 1523–1524). Presented at the 2005 IEEE International Joint Conference on Neural Networks, 2005., Montreal, QC, Canada: IEEE. https://doi.org/10.1109/IJCNN.2005.1556102

  24. Hikosaka O, Nakamura K, Sakai K, Nakahara H (2002) Central mechanisms of motor skill learning. Curr Opin Neurobiol 12(2):217–222. https://doi.org/10.1016/S0959-4388(02)00307-0

    Article  CAS  PubMed  Google Scholar 

  25. Hallgató E, Győri-Dani D, Pekár J, Janacsek K, Nemeth D (2013) The differential consolidation of perceptual and motor learning in skill acquisition. Cortex 49(4):1073–1081. https://doi.org/10.1016/j.cortex.2012.01.002

    Article  PubMed  Google Scholar 

  26. Conway CM (2020) How does the brain learn environmental structure? Ten core principles for understanding the neurocognitive mechanisms of statistical learning. Neurosci Biobehav Rev 112:279–299. https://doi.org/10.1016/j.neubiorev.2020.01.032

    Article  PubMed  PubMed Central  Google Scholar 

  27. Hikosaka O, Nakahara H, Rand MK, Sakai K, Lu X, Nakamura K, Doya K (1999) Parallel neural networks for learning sequential procedures. Trends Neurosci 22(10):464–471. https://doi.org/10.1016/S0166-2236(99)01439-3

    Article  CAS  PubMed  Google Scholar 

  28. Janacsek K, Shattuck KF, Tagarelli KM, Lum JAG, Turkeltaub PE, Ullman MT (2020) Sequence learning in the human brain: a functional neuroanatomical meta-analysis of serial reaction time studies. NeuroImage 207:116387. https://doi.org/10.1016/j.neuroimage.2019.116387

    Article  PubMed  Google Scholar 

  29. Brashers-Krug T, Shadmehr R, Bizzi E (1996) Consolidation in human motor memory. Nature 382(6588):252–255. https://doi.org/10.1038/382252a0

    Article  CAS  PubMed  Google Scholar 

  30. Robertson EM (2009) From creation to consolidation: a novel framework for memory processing. PLoS biology 7(1):e19. https://doi.org/10.1371/journal.pbio.1000019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Walker MP, Brakefield T, Allan Hobson J, Stickgold R (2003) Dissociable stages of human memory consolidation and reconsolidation. Nature 425(6958):616–620. https://doi.org/10.1038/nature01930

    Article  CAS  PubMed  Google Scholar 

  32. Baetens K, Firouzi M, Van Overwalle F, Deroost N (2020) Involvement of the cerebellum in the serial reaction time task (SRT) (Response to Janacsek et al.). NeuroImage 220:117114. https://doi.org/10.1016/j.neuroimage.2020.117114

    Article  PubMed  Google Scholar 

  33. Clark GM, Lum JAG, Ullman MT (2014) A meta-analysis and meta-regression of serial reaction time task performance in Parkinson’s disease. Neuropsychology 28(6):945–958. https://doi.org/10.1037/neu0000121

    Article  PubMed  Google Scholar 

  34. Clark GM, Lum JAG (2017) Procedural learning in Parkinson’s disease, specific language impairment, dyslexia, schizophrenia, developmental coordination disorder, and autism spectrum disorders: a second-order meta-analysis. Brain Cogn 117:41–48. https://doi.org/10.1016/j.bandc.2017.07.004

    Article  PubMed  Google Scholar 

  35. Hayes HA, Hunsaker N, Dibble LE (2015) Implicit motor sequence learning in individuals with Parkinson disease: a meta-analysis. J Parkinson’s Dis 5(3):549–560. https://doi.org/10.3233/JPD-140441

    Article  Google Scholar 

  36. Siegert RJ, Taylor KD, Weatherall M, Abernethy DA (2006) Is implicit sequence learning impaired in Parkinson’s disease? A meta-analysis. Neuropsychology 20(4):490–495. https://doi.org/10.1037/0894-4105.20.4.490

    Article  PubMed  Google Scholar 

  37. van Halteren-van Tilborg IADA, Scherder EJA, Hulstijn W (2007) Motor-skill learning in Alzheimer’s disease: a review with an eye to the clinical practice. Neuropsychol Rev 17(3):203–212. https://doi.org/10.1007/s11065-007-9030-1

    Article  PubMed  PubMed Central  Google Scholar 

  38. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, ... Moher D (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Int J Surg88:105906. https://doi.org/10.1136/bmj.n71

  39. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 62(10):e1–e34. https://doi.org/10.1016/j.jclinepi.2009.06.006

    Article  PubMed  Google Scholar 

  40. Dirnberger G, Novak J, Nasel C, Zehnter M (2010) Separating coordinative and executive dysfunction in cerebellar patients during motor skill acquisition. Neuropsychologia 48(5):1200–1208. https://doi.org/10.1016/j.neuropsychologia.2009.12.016

    Article  PubMed  Google Scholar 

  41. Dirnberger G, Novak J, Nasel C (2013) Perceptual sequence learning is more severely impaired than motor sequence learning in patients with chronic cerebellar stroke. J Cogn Neurosci 25(12):2207–2215. https://doi.org/10.1162/jocn_a_00444

    Article  PubMed  Google Scholar 

  42. Spencer RMC, Ivry RB (2009) Sequence learning is preserved in individuals with cerebellar degeneration when the movements are directly cued. J Cogn Neurosci 21(7):1302–1310. https://doi.org/10.1162/jocn.2009.21102

    Article  PubMed  PubMed Central  Google Scholar 

  43. Gomez-Beldarrain M, Garcia-Monco JC, Rubio B, Pascual-Leone A (1998) Effect of focal cerebellar lesions on procedural learning in the serial reaction time task. Exp Brain Res 120(1):25–30. https://doi.org/10.1007/s002210050374

    Article  CAS  PubMed  Google Scholar 

  44. Molinari M (1997) Cerebellum and procedural learning: evidence from focal cerebellar lesions. Brain 120(10):1753–1762. https://doi.org/10.1093/brain/120.10.1753

    Article  PubMed  Google Scholar 

  45. Pascual-Leone A, Grafman J, Clark K, Stewart M, Massaquoi S, Lou J-S, Hallett M (1993) Procedural learning in Parkinson’s disease and cerebellar degeneration. Ann Neurol 34(4):594–602. https://doi.org/10.1002/ana.410340414

    Article  CAS  PubMed  Google Scholar 

  46. Shin JC, Ivry RB (2003) Spatial and temporal sequence learning in patients with Parkinson’s disease or cerebellar lesions. J Cogn Neurosci 15(8):1232–1243. https://doi.org/10.1162/089892903322598175

  47. Tzvi E, Zimmermann C, Bey R, Münte TF, Nitschke M and Krämer UM (2017) Cerebellar degeneration affects cortico-cortical connectivity in motor learning networks. NeuroImage: Clin 16:66–78. https://doi.org/10.1016/j.nicl.2017.07.012

  48. Atkinson J, Braddick O (2011) From genes to brain development to phenotypic behavior: “dorsal-stream vulnerability” in relation to spatial cognition, attention, and planning of actions in Williams syndrome (WS) and other developmental disorders. Prog Brain Res 189:261–283. https://doi.org/10.1016/B978-0-444-53884-0.00029-4

    Article  PubMed  Google Scholar 

  49. Ferraro FR, Balota DA, Connor LT (1993) Implicit memory and the formation of new associations in nondemented Parkinson’s disease individuals and individuals with senile dementia of the Alzheimer type: a serial reaction time (SRT) investigation. Brain Cogn 21(2):163–180. https://doi.org/10.1006/brcg.1993.1013

    Article  CAS  PubMed  Google Scholar 

  50. Knopman D (1991) Long-term retention of implicitly acquired learning in patients with Alzheimer’s disease. J Clin Exp Neuropsychol 13(6):880–894. https://doi.org/10.1080/01688639108405105

    Article  CAS  PubMed  Google Scholar 

  51. Schmitz X, Bier N, Joubert S, Lejeune C, Salmon E, Rouleau I, Meulemans T (2014) The Benefits of errorless learning for serial reaction time performance in Alzheimer’s disease. J Alzheimer’s Dis 39(2):287–300. https://doi.org/10.3233/JAD-130887

    Article  Google Scholar 

  52. van Tilborg IADA, Hulstijn W (2010) Implicit motor learning in patients with Parkinson’s and Alzheimer’s disease: differences in learning abilities? Mot Control 14(3):344–361. https://doi.org/10.1123/mcj.14.3.344

    Article  Google Scholar 

  53. Willingham DB, Peterson EW, Manning C, Brashear HR (1997) Patients with Alzheimer’s disease who cannot perform some motor skills show normal learning of other motor skills. Neuropsychology 11(2):261–271. https://doi.org/10.1037/0894-4105.11.2.261

    Article  CAS  PubMed  Google Scholar 

  54. Kemény F, Demeter G, Racsmány M, Valálik I, Lukács Á (2019) Impaired sequential and partially compensated probabilistic skill learning in Parkinson’s disease. J Neuropsychol 13(3):509–528. https://doi.org/10.1111/jnp.12163

    Article  PubMed  Google Scholar 

  55. Sommer M, Grafman J, Clark K, Hallett M (1999) Learning in Parkinson’s disease: eyeblink conditioning, declarative learning, and procedural learning. J Neurol Neurosurg Psychiatry 67(1):27–34. https://doi.org/10.1136/jnnp.67.1.27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Stefanova ED, Kostic VS, Ziropadja L, Markovic M, Ocic GG (2000) Visuomotor skill learning on serial reaction time task in patients with early Parkinson’s disease. Mov Disord 15(6):9

    Article  Google Scholar 

  57. Stephan MA, Meier B, Zaugg SW, Kaelin-Lang A (2011) Motor sequence learning performance in Parkinson’s disease patients depends on the stage of disease. Brain Cogn 75(2):135–140. https://doi.org/10.1016/j.bandc.2010.10.015

    Article  PubMed  Google Scholar 

  58. Dominey PF, Ventre-Dominey J, Broussolle E, Jeannerod M (1997) Analogical transfer is effective in a serial reaction time task in Parkinson’s disease: evidence for a dissociable form of sequence learning. Neuropsychologia 35(1):1–9. https://doi.org/10.1016/S0028-3932(96)00050-4

    Article  CAS  PubMed  Google Scholar 

  59. Pascual-Leone A, Valls-Sole J, Brasil-Neto JP, Cammarota A, Grafman J, Hallett M (1994) Akinesia in Parkinson’s disease. II. Effects of subthreshold repetitive transcranial motor cortex stimulation. Neurology 44(5):892–892. https://doi.org/10.1212/WNL.44.5.892

    Article  CAS  PubMed  Google Scholar 

  60. Kwak Y, Müller MLTM, Bohnen NI, Dayalu P, Seidler RD (2010) Effect of dopaminergic medications on the time course of explicit motor sequence learning in Parkinson’s disease. J Neurophysiol 103(2):942–949. https://doi.org/10.1152/jn.00197.2009

    Article  CAS  PubMed  Google Scholar 

  61. Meissner SN, Krause V, Südmeyer M, Hartmann CJ and Pollok B (2018) The significance of brain oscillations in motor sequence learning: insights from Parkinson’s disease. NeuroImage: Clin 20:448–457. https://doi.org/10.1016/j.nicl.2018.08.009

  62. Seidler RD, Tuite P, Ashe J (2007) Selective impairments in implicit learning in Parkinson’s disease. Brain Res 1137(1):104–110. https://doi.org/10.1016/j.brainres.2006.12.057

    Article  CAS  PubMed  Google Scholar 

  63. Wang XP, Sun BM, Ding HL (2009) Changes of procedural learning in Chinese patients with non-demented Parkinson disease. Neurosci Lett 449(3):161–163. https://doi.org/10.1016/j.neulet.2008.10.086

  64. Helmuth LL, Mayr U, Daum I (2000) Sequence learning in Parkinson’s disease: a comparison of spatial-attention and number-response sequences. Neuropsychologia 38(11):1443–1451. https://doi.org/10.1016/S0028-3932(00)00059-2

    Article  CAS  PubMed  Google Scholar 

  65. Schmahmann JD, Guell X, Stoodley CJ, Halko MA (2019) The theory and neuroscience of cerebellar cognition. Annu Rev Neurosci 42(1):337–364. https://doi.org/10.1146/annurev-neuro-070918-050258

    Article  CAS  PubMed  Google Scholar 

  66. Ito M (2008) Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci 9(4):304–313. https://doi.org/10.1038/nrn2332

    Article  CAS  PubMed  Google Scholar 

  67. Diedrichsen J, King M, Hernandez-Castillo C, Sereno M, Ivry RB (2019) Universal transform or multiple functionality? Understanding the contribution of the human cerebellum across task domains. Neuron 102(5):918–928. https://doi.org/10.1016/j.neuron.2019.04.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Knopman DS, Nissen MJ (1987) Implicit learning in patients with probable Alzheimer’s disease. Neurology 37(5):784–784. https://doi.org/10.1212/WNL.37.5.784

    Article  CAS  PubMed  Google Scholar 

  69. Muslimovic D, Post B, Speelman JD, Schmand B (2007) Motor procedural learning in Parkinson’s disease. Brain 130(11):2887–2897. https://doi.org/10.1093/brain/awm211

    Article  CAS  PubMed  Google Scholar 

  70. Deroost N, Kerckhofs E, Coene M, Wijnants G, Soetens E (2006) Learning sequence movements in a homogenous sample of patients with Parkinson’s disease. Neuropsychologia 44(10):1653–1662. https://doi.org/10.1016/j.neuropsychologia.2006.03.021

    Article  PubMed  Google Scholar 

  71. Meissner SN, Krause V, Südmeyer M, Hartmann CJ and Pollok B (2019) Pre-stimulus beta power modulation during motor sequence learning is reduced in ’Parkinson’s disease. NeuroImage: Clin 24:102057. https://doi.org/10.1016/j.nicl.2019.102057

  72. Vandenbossche J, Deroost N, Soetens E, Coomans D, Spildooren J, Vercruysse S, Kerckhofs E (2013) Impaired implicit sequence learning in Parkinson’s disease patients with freezing of gait. Neuropsychology 27(1):28–36. https://doi.org/10.1037/a0031278

    Article  PubMed  Google Scholar 

  73. Kelly SW, Jahanshahi M, Dirnberger G (2004) Learning of ambiguous versus hybrid sequences by patients with Parkinson’s disease. Neuropsychologia 42(10):1350–1357. https://doi.org/10.1016/j.neuropsychologia.2004.02.013

    Article  PubMed  Google Scholar 

  74. Werheid K, Zysset S, Müller A, Reuter M, von Cramon DY (2003a) Rule learning in a serial reaction time task: An fMRI study on patients with early Parkinson’s disease. Cogn Brain Res 16(2):273–284. https://doi.org/10.1016/S0926-6410(02)00283-5

    Article  Google Scholar 

  75. Werheid K, Ziessler M, Nattkemper D, Yves von Cramon D (2003b) Sequence learning in Parkinson’s disease: The effect of spatial stimulus-response compatibility. Brain and Cognition 52(2):239–249. https://doi.org/10.1016/s0278-2626(03)00076-9

  76. Fisher BE, Morton SM, Lang CE (2014) From motor learning to physical therapy and back again: the state of the art and science of motor learning rehabilitation research. J Neurol Phys Ther 38(3):149–150. https://doi.org/10.1097/NPT.0000000000000043

    Article  PubMed  PubMed Central  Google Scholar 

  77. Grafman J, Weingartner H, Newhouse PA, Thompson K, Lalonde F, Litvan I, Molchan S, Sunderland T (1990) Implicit learning in patients with Alzheimer’s disease. Pharmacopsychiatry 23(2):94–101. https://doi.org/10.1055/s-2007-1014490

  78. Gawrys L, Szatkowska I, Jamrozik Z, Janik P, Friedman A, Kaczmarek L (2008) Nonverbal deficits in explicit and implicit memory of Parkinson’s disease patients. Acta Neurobiol Exp 68(1):58–72

  79. Jackson GM, Jackson SR, Harrison J, Henderson L, Kennard C (1995) Serial reaction time learning and Parkinson’s disease: Evidence for a procedural learning deficit. Neuropsychologia 33(5):577–593. https://doi.org/10.1016/0028-3932(95)00010-z

  80. Ghilardi M-F, Eidelberg D, Silvestri G, Ghez C (2003) The differential effect of PD and normal aging on early explicit sequence learning. Neurology 60(8):1313–1319. https://doi.org/10.1212/01.wnl.0000059545.69089.ee

  81. Kwak Y, Müller MLTM, Bohnen NI, Dayalu P, Seidler RD (2010) Effect of dopaminergic medications on the time course of explicit motor sequence learning in Parkinson’s disease. J Neurophysiol 103(2):942–949. https://doi.org/10.1152/jn.00197.2009

  82. Tzvi E, Bey R, Nitschke M, Brüggemann N, Classen J, Münte TF, Krämer UM, Rumpf J-J (2021) Motor sequence learning deficits in idiopathic parkinson’s disease are associated with increased substantia nigra activity. Front Aging Neurosci 13:685168. https://doi.org/10.3389/fnagi.2021.685168

  83. Brown RG, Jahanshahi M, Limousin-Dowsey P, Thomas D, Quinn NP, Rothwell JC (2003) Pallidotomy and incidental sequence learning in Parkinson’s disease: NeuroReport 14(1):21–24. https://doi.org/10.1097/00001756-200301200-00004

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elodie Martin.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 62 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martin, E., Scotté-Barranoff, C. & Tallet, J. What neurological diseases tell us about procedural perceptual-motor learning? A systematic review of the literature. Neurol Sci 44, 2645–2665 (2023). https://doi.org/10.1007/s10072-023-06724-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-023-06724-w

Keywords

Navigation