A meta-analysis and meta-regression of serial reaction time task performance in Parkinson's disease

Neuropsychology

Volumn 28, Issue 6, 2014, Pages 945-958

  Clark, Gillian M ^a   Lum, Jarrad A G ^a   Ullman, Michael T ^b  

^a DEAKIN UNIVERSITY   (Australia)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Implicit learning; Metaanalysis; Parkinson's disease; Procedural learning; Serial reaction time (RT)

Indexed keywords

ARTICLE; DISEASE SEVERITY; EFFECT SIZE; HUMAN; LEARNING; LITERATURE; META ANALYSIS; PARKINSON DISEASE; PRIORITY JOURNAL; PROCEDURAL MEMORY; REACTION TIME; REGRESSION ANALYSIS; SEQUENCE LEARNING; SERIAL REACTION TIME; TASK PERFORMANCE; COMPLICATION; LEARNING DISORDERS; MEMORY; MEMORY DISORDERS; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PSYCHOLOGY; SEVERITY OF ILLNESS INDEX;

HUMANS; LEARNING; LEARNING DISORDERS; MEMORY; MEMORY DISORDERS; NEUROPSYCHOLOGICAL TESTS; PARKINSON DISEASE; REACTION TIME; REGRESSION ANALYSIS; SEVERITY OF ILLNESS INDEX; TASK PERFORMANCE AND ANALYSIS;

EID: 84925833605     PISSN: 08944105     EISSN: 19311559     Source Type: Journal    
DOI: 10.1037/neu0000121     Document Type: Article

References (85)

1. *Bondi, M. W. (1991). Neurobehavioural functioning in Parkinson's disease:The role of basal ganglia-thalamocortical circuit loops in predicting performance. (Doctor of Philosophy), The University of Arizona, Tucson, AZ.
2. Borenstein, M., Hedges, L. V., Higgins, J. P. T., & Rothstein, H. R. (2005). Comprehensive meta-analysis (Version 2). Englewood, NJ: Biostat.
3. Borenstein, M., Hedges, L. V., Higgins, J. P. T., & Rothstein, H. R. (2011). Introduction to meta-analysis. Hoboken, NJ: Wiley.
4. *Brown, R. G., Jahanshahi, M., Limousin-Dowsey, P., Thomas, D., Quinn, N. P., & Rothwell, J. C. (2003). Pallidotomy and incidental sequence learning in Parkinson's disease. NeuroReport, 14, 21-24. doi:10.1097/ 00001756-200301200-00004
5. Brown, R. G., & Marsden, C. D. (1991). Dual task performance and processing resources in normal subjects and patients with Parkinson's disease. Brain, 114, 215-231.
6. *Cameli, L. (2006). Memory and language: Insights from picture description and past tense generation in a native and a second language in bilingual Alzheimer and Parkinson patients. (Doctor of Philosophy), Concordia University, Portland, Oregon.
7. Cohen, A., Ivry, R. I., & Keele, S. W. (1990). Attention and structure in sequence learning. Journal of Experimental Psychology: Learning, Memory, and Cognition, 16, 17-30. doi:10.1037/0278-7393.16.1.17
8. Cohen, J. (1988). Statistical power analysis for the behavioral sciences. Hillsdale, NJ: Laurence Erlbaum.
9. Cooper, J. A., Sagar, H. J., Jordan, N., Harvey, N. S., & Sullivan, E. V. (1991). Cognitive impairment in early, untreated Parkinson's disease and its relationship to motor disability. Brain, 114, 2095-2122. doi:10.1093/brain/114.5.2095
10. Curran, T. (1997). Higher-order associative learning in amnesia: Evidence from the serial reaction time task. Journal of Cognitive Neuroscience, 9, 522-533. doi:10.1162/jocn.1997.9.4.522
11. Dalrymple-Alford, J. C., Kalders, A. S., Jones, R. D., & Watson, R. W. (1994). A central executive deficit in patients with Parkinson's disease. Journal of Neurology, Neurosurgery & Psychiatry, 57, 360-367. doi:10.1136/jnnp.57.3.360
12. *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, 1653-1662. doi:10.1016/j.neuropsychologia.2006.03.021
13. Dubois, B., & Pillon, B. (1996). Cognitive deficits in Parkinson's disease. Journal of Neurology, 244, 2-8. doi:10.1007/PL00007725
14. Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997). Bias in meta-analysis detected by a simple, graphical test. British Medical Journal, 315, 629-634. doi:10.1136/bmj.315.7109.629
15. Ergorul, C., & Eichenbaum, H. (2006). Essential role of the hippocampal formation in rapid learning of higher-order sequential associations. The Journal of Neuroscience, 26, 4111-4117. doi:10.1523/JNEUROSCI .0441-06.2006
16. *Ferraro, F. R., Balota, D. A., & Connor, L. T. (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 and Cognition, 21, 163-180. doi:10.1006/brcg.1993.1013
17. Foerde, K., Knowlton, B. J., & Poldrack, R. A. (2006). Modulation of competing memory systems by distraction. Proceedings of the National Academy of Sciences, 103, 11778-11783.
18. *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 Neurobiologiae Experimentalis, 68, 58-72.
19. *Gilbert, B. (2003). Working memory and procedural memory in Parkinson's disease: Evaluation and training. (Doctor of Philosophy), University of Montreal, Montreal, Canada.
20. Gray, H. M., & Tickle-Degnen, L. (2010). A meta-analysis of performance on emotion recognition tasks in Parkinson's disease. Neuropsychology, 24, 176-191. doi:10.1037/a0018104
21. Greenland, S. (1987). Quantitative methods in the review of epidemiologic literature. Epidemiologic Reviews, 9, 1-30.
22. Hardwick, R. M., Rottschy, C., Miall, R. C., & Eickhoff, S. B. (2013). A quantitative meta-analysis and review of motor learning in the human brain. NeuroImage, 67, 283-297. doi:10.1016/j.neuroimage.2012.11.020
23. Hedges, L. V., & Olkin, I. (1985). Statistical methods for meta-analysis. Orlando, FL: Academic Press.
24. Helkala, E., Laulumaa, V., Soininen, H., & Riekkinen, P. J. (1988). Recall and recognition memory in patients with Alzheimer's and Parkinson's diseases. Annals of Neurology, 24, 214-217. doi:10.1002/ana .410240207
25. *Helmuth, L. L., Mayr, U., & Daum, I. (2000). Sequence learning in Parkinson's disease: A comparison of spatial-attention and numberresponse sequences. Neuropsychologia, 38, 1443-1451. doi:10.1016/S0028-3932(00)00059-2
26. Higgins, J., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003). Measuring inconsistency in meta-analyses. British Medical Journal, 327, 557-560. doi:10.1136/bmj.327.7414.557
27. Hoehn, M. M., & Yahr, M. D. (1967). Parkinsonism: Onset, progression, and mortality. Neurology, 17, 427-442.
28. Hunter, J. E., Schmidt, F. L., & Jackson, G. B. (1982). Meta-analysis. Beverly Hills, CA: Sage Publications.
29. *Jackson, G. M., Jackson, S. R., Harrison, J., Henderson, L., & Kennard, C. (1995). Serial reaction time learning and Parkinson's disease: Evidence for a procedural learning deficit. Neuropsychologia, 33, 577-593. doi:10.1016/0028-3932(95)00010-Z
30. Jankovic, J. (2008). Parkinson's disease: Clinical features and diagnosis. Journal of Neurology, Neurosurgery & Psychiatry, 79, 368-376. doi:10.1136/jnnp.2007.131045
31. Kandel, E. R., Schwartz, J. H., & Jessell, T. M. (2012). Principles of neural science. (5th ed.). New York, NY: McGraw-Hill.
32. *Kelly, S. W., Jahanshahi, M., & Dirnberger, G. (2004). Learning of ambiguous versus hybrid sequences by patients with Parkinson's disease. Neuropsychologia, 42, 1350-1357. doi:10.1016/j.neuropsychologia. 2004.02.013
33. Knopman, D., & Nissen, M. J. (1991). Procedural learning is impaired in Huntington's disease: Evidence from the serial reaction time task. Neuropsychologia, 29, 245-254. doi:10.1016/0028-3932(91)90085-M
34. Knowlton, B. J., Mangels, J. A., & Squire, L. R. (1996). A neostriatal habit learning system in humans. Science, 273, 1399-1402. doi:10.1126/ science.273.5280.1399
35. Knowlton, B. J., Squire, L. R., & Gluck, M. A. (1994). Probabilistic classification learning in amnesia. Learning & Memory, 1, 106-120.
36. Kudlicka, A., Clare, L., & Hindle, J. V. (2011). Executive functions in Parkinson's disease: A systematic review and meta-analysis. Movement Disorders, 26, 2305-2315. doi:10.1002/mds.23868
37. Lang, A. E., & Lozano, A. M. (1998). Parkinson's disease. The New England Journal of Medicine, 339, 1044-1053. doi:10.1056/NEJM199810083391506
38. Lozano, A. M., Lang, A. E., Galvez-Jimenez, N., Miyasaki, J., Duff, J., Hutchison, W. D., & Dostrovsky, J. O. (1995). Effect of GPi pallidotomy on motor function in Parkinson's disease. The Lancet, 346, 1383-1387. doi:10.1016/S0140-6736(95)92404-3
39. Lum, J. A. G., & Kidd, E. (2012). An examination of the associations among multiple memory systems, past tense, and vocabulary in typically developing 5-year-old children. Journal of Speech, Language and Hearing Research, 55, 989-1006. doi:10.1044/1092-4388(2011/10-0137)
40. Lum, J. A. G., Ullman, M. T., & Conti-Ramsden, G. (2013). Procedural learning is impaired in dyslexia: Evidence from a meta-analysis of serial reaction time studies. Research in Developmental Disabilities, 34, 3460-3476. doi:10.1016/j.ridd.2013.07.017
41. Mayes, A., Montaldi, D., & Migo, E. (2007). Associative memory and the medial temporal lobes. Trends in Cognitive Sciences, 11, 126-135. doi:10.1016/j.tics.2006.12.003
42. Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & The PRISMA Group. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Medicine, 6. doi:10.1371/ journal.pmed.1000097
43. *Muslimovic, D., Post, B., Speelman, J. D., & Schmand, B. (2007). Motor procedural learning in Parkinson's disease. Brain, 130, 2887-2897. doi:10.1093/brain/awm211
44. Nissen, M. J., & Bullemer, P. (1987). Attentional requirements of learning:Evidence from performance measures. Cognitive Psychology, 19, 1-32. doi:10.1016/0010-0285(87)90002-8
45. Owen, A. M., Iddon, J. L., Hodges, J. R., Summers, B. A., & Robbins, T. W. (1997). Spatial and non-spatial working memory at different stages of Parkinson's disease. Neuropsychologia, 35, 519-532. doi:10.1016/S0028-3932(96)00101-7
46. Packard, M. G., & Knowlton, B. J. (2002). Learning and memory functions of the basal ganglia. Annual Review of Neuroscience, 25, 563-593. doi:10.1146/annurev.neuro.25.112701.142937
47. Parent, A., & Hazrati, L. (1995). Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Research Reviews, 20, 91-127. doi:10.1016/0165-0173(94)00007-C
48. *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. Annals of Neurology, 34, 594-602. doi:10.1002/ana.410340414
49. Pascual-Leone, A., Valls-Sole, J., Brasil-Neto, J. P., Cammarota, A., Grafman, J., & Hallett, M. (1994). Akinesia in Parkinson's disease. II. Effects of subthreshold repetitive transcranial motor cortex stimulation. Neurology, 44, 892-898. doi:10.1212/WNL.44.5.892
50. Pascual-Leone, A., Wassermann, E. M., Grafman, J., & Hallett, M. (1996). The role of the dorsolateral prefrontal cortex in implicit procedural learning. Experimental Brain Research, 107, 479-485. doi:10.1007/BF00230427
51. Poldrack, R. A., & Rodriguez, P. (2003). Sequence learning: What's the hippocampus to do?. Neuron, 37, 891-893. doi:10.1016/S0896-6273(03)00159-4
52. Price, A., & Shin, J. C. (2009). The impact of Parkinson's disease on sequence learning: Perceptual pattern learning and executive function. Brain & Cognition, 69, 252-261. doi:10.1016/j.bandc.2008.07.013
53. Robertson, E. M. (2007). The serial reaction time task: Implicit motor skill learning?. The Journal of Neuroscience, 27, 10073-10075. doi:10.1523/JNEUROSCI.2747-07.2007
54. *Sarazin, M., Deweer, B., Pillon, B., Merkl, A., & Dubois, B. (2001). Procedural learning and Parkinson's disease: Implications of the striatofrontal loops. Revue Neurologique, 157, 1513-1518.
55. Schendan, H. E., Searl, M. M., Melrose, R. J., & Stern, C. E. (2003). An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron, 37, 1013-1025. doi:10.1016/S0896-6273(03)00123-5
56. *Seidler, R. D., Tuite, P., & Ashe, J. (2007). Selective impairments in implicit learning in Parkinson's disease. Brain Research, 1137, 104-110. doi:10.1016/j.brainres.2006.12.057
57. *Selco, S. L. (1998). The nature of the processes, representations, and neural substrates which support and contribute to motor sequence learning. (Doctor of Philosophy), University of Illinois, Champaign, IL.
58. *Shin, J. C., & Ivry, R. B. (2003). Spatial and temporal sequence learning in patients with Parkinson's disease or cerebellar lesions. Journal of Cognitive Neuroscience, 15(8), 1232-1243. doi:10.1162/ 089892903322598175
59. Siegert, R., Taylor, K. D., Weatherall, M., & Abernethy, D. (2006). Is implicit sequence learning impaired in Parkinson's disease? A metaanalysis. Neuropsychology, 20, 490-495. doi:10.1037/0894-4105.20.4.490
60. Siegert, R., Weatherall, M., & Bell, E. M. (2008). Is implicit sequence learning impaired in schizophrenia? A meta-analysis. Brain and Cognition, 67, 351-359. doi:10.1016/j.bandc.2008.02.005
61. Siegert, R., Weatherall, M., Taylor, K. D., & Abernethy, D. (2008). A meta-analysis of performance on simple span and more complex working memory tasks in Parkinson's disease. Neuropsychology, 22, 450-461. doi:10.1037/0894-4105.22.4.450
62. *Smith, J. G., & McDowall, J. (2004). Impaired higher order implicit sequence learning on the verbal version of the serial reaction time task in patients with Parkinson's disease. Neuropsychology, 18, 679-691. doi:10.1037/0894-4105.18.4.679
63. *Smith, J. G., & McDowall, J. (2006). The implicit sequence learning deficit in patients with Parkinson's disease: A matter of impaired sequence integration?. Neuropsychologia, 44, 275-288. doi:10.1016/j .neuropsychologia.2005.05.001
64. *Smith, J. G., Siegert, R., McDowall, J., & Abernethy, D. (2001). Preserved implicit learning on both the serial reaction time task and artificial grammar in patients with Parkinson's disease. Brain and Cognition, 45, 378-391. doi:10.1006/brcg.2001.1286
65. *Sommer, M., Grafman, J., Clark, K., & Hallett, M. (1999). Learning in Parkinson's disease: Eyeblink conditioning, declarative learning, and procedural learning. Journal of Neurology, Neurosurgery and Psychiatry, 67, 27-34. doi:10.1136/jnnp.67.1.27
66. Squire, L. R. (2004). Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory, 82, 171-177. doi:10.1016/j.nlm.2004.06.005
67. Squire, L. R., Knowlton, B. J., & Musen, G. (1993). The structure and organization of memory. Annual Review of Psychology, 44, 453-495. doi:10.1146/annurev.ps.44.020193.002321
68. Squire, L. R., Stark, C. E. L., & Clark, R. E. (2004). The medial temporal lobe. Annual Review of Neuroscience, 27, 279-306. doi:10.1146/ annurev.neuro.27.070203.144130
69. Squire, L. R., & Zola, S. M. (1996). Structure and function of declarative and nondeclarative memory systems. Proceedings of the National Academy of Sciences of the United States of America, 93, 13515-13522. doi:10.1073/pnas.93.24.13515
70. *Stefanova, E. D., Kostic, V. S., Ziropadja, L., Markovic, M., & Ocic, G. G. (2000). Visuomotor skill learning on serial reaction time task in patients with early Parkinson's disease. Movement Disorders, 15, 1095-1103. doi:10.1002/1531-8257(200011)15:6_1095::AID-MDS1006_3.0.CO;2-R
71. Thomas, K. M., Hunt, R. H., Vizueta, N., Sommer, T., Durston, S., Yang, Y., & Worden, M. S. (2004). Evidence of developmental differences in implicit sequence learning: An fMRI study of children and adults. Journal of Cognitive Neuroscience, 16, 1339-1351. doi:10.1162/ 0898929042304688
72. Thomas, K. M., & Nelson, C. A. (2001). Serial reaction time learning in preschool-and school-age children. Journal of Experimental Child Psychology, 79, 364-387. doi:10.1006/jecp.2000.2613
73. Thompson, S. G., & Higgins, J. P. (2002). How should meta-regression analyses be undertaken and interpreted?. Statistics in Medicine, 21, 1559-1573. doi:10.1002/sim.1187
74. Ullman, M. T. (2001). A neurocognitive perspective on language: The declarative/procedural model. Nature Reviews Neuroscience, 2, 717-726. doi:10.1038/35094573
75. Ullman, M. T. (2004). Contributions of memory circuits to language: The declarative/procedural model. Cognition, 92, 231-270. doi:10.1016/j .cognition.2003.10.008
76. Ullman, M. T. (2006). Is Broca's area part of a basal ganglia thalamocortical circuit?. Cortex, 42, 480-485. doi:10.1016/S0010-9452(08)70382-4
77. Ullman, M. T., Corkin, S., Coppola, M., Hickok, G., Growdon, J. H., Koroshetz, W. J., & Pinker, S. (1997). A neural dissociation within language: Evidence that the mental dictionary is part of declarative memory, and that grammatical rules are processed by the procedural system. Journal of Cognitive Neuroscience, 9, 266-276. doi:10.1162/ jocn.1997.9.2.266
78. *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, 28-36. doi:10.1037/a0031278
79. *van Tilborg, I., & Hulstijn, W. (2010). Implicit motor learning in patients with Parkinson's and Alzheimer's disease: Differences in learning abilities?. Motor Control, 14, 344-361.
80. *Wang, X. P., Sun, B. M., & Ding, H. L. (2009). Changes of procedural learning in Chinese patients with non-demented Parkinson disease. Neuroscience Letters, 449, 161-163. doi:10.1016/j.neulet.2008.10.086
81. *Werheid, K., Ziessler, M., Nattkemper, D., & Von Cramon, D. Y. (2003). Sequence learning in Parkinson's disease: The effect of spatial stimulusresponse compatibility. Brain and Cognition, 52, 239-249. doi:10.1016/S0278-2626(03)00076-9
82. *Werheid, K., Zysset, S., Muller, A., Reuter, M., & Von Cramon, D. Y. (2003). Rule learning in a serial reaction time task: An fMRI study on patients with early Parkinson's disease. Cognitive Brain Research, 16, 273-284. doi:10.1016/S0926-6410(02)00283-5
83. *Westwater, H., McDowall, J., Siegert, R., Mossman, S., & Abernethy, D. (1998). Implicit learning in Parkinson's disease: Evidence from a verbal version of the serial reaction time task. Journal of Clinical and Experimental Neuropsychology, 20, 413-418. doi:10.1076/jcen.20.3.413.826
84. Wu, T., & Hallett, M. (2008). Neural correlates of dual task performance in patients with Parkinson's disease. Journal of Neurology, Neurosurgery and Psychiatry, 79, 760-766. doi:10.1136/jnnp.2007.126599
85. Yin, H. H., & Knowlton, B. J. (2006). The role of the basal ganglia in habit formation. Nature Reviews Neuroscience, 7, 464-476. doi:10.1038/ nrn1919