Neural evidence of a role for spatial response selection in the learning of spatial sequences

Brain Research

Volumn 1247, Issue , 2009, Pages 114-125

  Schwarb, Hillary ^a   Schumacher, Eric H ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Functional imaging; Hippocampus; Prefrontal cortex; Sequence learning; Serial reaction time (SRT) task; Supplementary motor area

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; BRAIN MAPPING; BRAIN REGION; CAUDATE NUCLEUS; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; ERROR; FEEDBACK SYSTEM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; LEARNING; MALE; NERVE CONDUCTION; NEUROIMAGING; NORMAL HUMAN; ORIENTING RESPONSE; PARIETAL LOBE; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIORITY JOURNAL; PUTAMEN; REACTION TIME; RESPONSE TIME; SEQUENCE LEARNING; SPATIAL ORIENTATION; STIMULUS RESPONSE; TASK PERFORMANCE;

ADOLESCENT; ADULT; BRAIN MAPPING; CEREBRAL CORTEX; DECISION MAKING; FEMALE; HUMANS; LEARNING; MAGNETIC RESONANCE IMAGING; MALE; MOTOR CORTEX; NEURAL PATHWAYS; NEURONS; NEUROPSYCHOLOGICAL TESTS; ORIENTATION; PHOTIC STIMULATION; PREFRONTAL CORTEX; REACTION TIME; SPACE PERCEPTION; TIME FACTORS; YOUNG ADULT;

EID: 57349182207     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.09.097     Document Type: Article

References (77)

1. American Psychological Association. Ethical principles of psychologists and code of conduct. Am. Psychol. 40 (1992) 1597-1611
2. Bischoff-Grethe A., Geodert K.M., Willingham D.T., and Grafton S.T. Neural substrates of response-based sequence learning using fMRI. J. Cognit. Neurosci. 16 (2004) 127-138
3. Botvinick M.M., Braver T.S., Barch D.M., Carter C.S., and Cohen J.D. Conflict monitoring and cognitive control. Psychol. Rev. 108 (2001) 624-652
4. Botvinick M.M., Cohen J.D., and Carter C.S. Conflict monitoring and anterior cingulate cortex: an update. Trends Cognit. Sci. 8 (2004) 539-546
5. Bracewell R.M., Mazzoni P., Barash S., and Anderson R.A. Motor intention activity in the macaque's lateral intraparietal area 0.2. Changes in motor plan. J. Neurophysiol. 76 (1996) 1457-1464
6. Clegg B.A. Stimulus-specific sequence representation in serial reaction time tasks. Q. J. Exp. Psychol. 58A (2005) 1087-1101
7. Cohen A., Ivry R.I., and Keele S.W. Attention and structure in sequence learning. J. Exp. Psychol. Learn Mem. Cognit. 16 (1990) 17-30
8. Cohen N.J., and Eichenbaum H. Memory, Amnesia, and the Hippocampal System (1993), MIT Press, Cambridge, MA.
9. Curtis C., and D'Esposito M. Persistent activity in the prefrontal cortex during working memory. Trends Cognit. Sci. 7 (2003) 415-423
10. Dassonville P., Lewis S.M., Zhu X.H., Ugurbil K., Kim S.G., and Ashe J. The effect of stimulus-response compatibility on cortical motor activation. NeuroImage 13 (2001) 1-14
11. Deroost N., and Soetens E. The role of response selection in sequence learning. Q. J. Exp. Psychol. 59 (2006) 449-456
12. Destrebecqz A., Peigneux P., Laureys S., Degueldre C., Del Fiore G., Aerts J.1., Luxen A., Van Der Linden M., Cleeremans A., and Maquet P. The neural correlates of implicit and explicit sequence learning: interacting networks revealed by the process dissociation procedure. Learn Mem. 12 (2005) 480-490
13. di Pellegrino G., and Wise S.P. Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate. J. Neurosci. 13 (1993) 1227-1243
14. Duncan J. Response selection rules in spatial choice reaction tasks. In: Dornic S. (Ed). Attention and Performance VI (1977), Lawrence Erlbaum Associates, Publishers, Hillsdale, New Jersey 49-61
15. Eliassen J.C., Souza T., and Sanes J.N. Human brain activation accompanying explicitly irected movement sequence learning. Exp. Brain Res. 141 (2001) 269-280
16. Fitts P.M., and Seeger C.M. S-R compatibility: spatial characteristics of stimulus and response codes. J. Exp. Psychol. 46 (1953) 199-210
17. Fortin N.J., Agster K.L., and Eichenbaum H.B. Critical role of the hippocampus in memory for sequences of events. Nat. Neurosci. 5 (2002) 458
18. Frensch P.A., Wenke D., and Runger D. A secondary tone-counting task suppresses expression of knowledge in the serial reaction task. J. Exp. Psychol. Learn Mem. Cognit. 25 (1999) 260-274
19. Friston K.J., Ashburner J., Frith C.D., Poline J.-B., Heather J.D., and Frackowiak R.S.J. Spatial registration and normalization of images. Hum. Brain Mapp. 2 (1995) 165-189
20. Grafton S.T., Mazziotta J.C., Presty S., Friston K.J., Frackowiak R.S.J., and Phelps M.E. Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J. Neurosci. 12 (1992) 2542-2548
21. Grafton S.T., Hazeltine E., and Ivry R. Functional mapping of sequence learning in normal humans. J. Cognit. Neurosci. 7 (1995) 497-510
22. Grafton S.T., Hazeltine E., and Ivry R.B. Abstract and effector-specific representations of motor sequences identified with PET. J. Neurosci. 18 (1998) 9420-9428
23. Grafton S.T., Salidis J., and Willingham D.B. Motor learning of compatible and incompatible visuomotor maps. J. Cognit. Neurosci. 13 (2001) 217-231
24. Grafton S.T., Hazeltine E., and Ivry R.B. Motor sequence learning with the nondominant left hand. Exp. Brain Res. 146 (2002) 369-378
25. Hazeltine E. The representational nature of sequence learning: evidence for goal-based codes. In: Prinz W., and Hommel B. (Eds). Attention and Performance 14 (2002), University Press, Oxford 673-689
26. Hazeltine E., Grafton S.T., and Ivry R. Attention and stimulus characteristics determine the locus of motor-sequence encoding a PET study. Brain 120 (1997) 123-140
27. Honda M., Deiber M.P., Ibanez V., Pascual-Leone A., Zhuang P., and Hallett M. Dynamic cortical involvement in implicit and explicit motor sequence learning. A PET study. Brain 121 (1998) 2159-2173
28. Howard J.H., Mutter S.A., and Howard D.V. Serial pattern learning by event observation. J. Exp. Psychol. Learn Mem. Cognit. 18 (1992) 1029-1039
29. Iacoboni M., Woods R.P., and Mazziotta J.C. Brain-behavior relationships: evidence from practice effects in spatial stimulus-response compatibility. J. Neurophysiol. 76 (1996) 321-331
30. Jahanshahi M., Jenkins I.H., Brown R.G., Marsden C.D., Passingham R.E., and Brooks D.J. Self-initiated versus externally triggered movements: I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects. Brain 118 (1995) 913-933
31. Jenkins I.H., Brooks D.J., Nixon P.D., Frackowiak R.S.J., and Passingham R.E. Motor sequence learning: a study with positron emmission tomography. J. Neurosci. 14 (1994) 3775-3790
32. Jiang Y., and Kanwisher N. Common neural substrates for response selection across modalities and mapping paradigms. J. Cognit. Neurosci. 15 (2003) 1080-1094
33. Kleinbaum D.G., Kupper L.L., Muller K.E., and Nizam A. Applied Regression Analysis and Other Multivariable Methods (1998), Brooks. Cole Publishing Company, Pacific Grove, CA
34. Kornblum S., Hasbroucq T., and Osman A. Dimensional overlap: cognitive basis for stimulus-response compatibility - a model and taxonomy. Psychol. Rev. 97 (1990) 253-270
35. Laforce Jr. R. Distinct contribution of the striatum and cerebellum to motor learning. Brain Cognit. 45 (2001) 189-211
36. Laforce Jr. R. Revue des mécanismes d'apprentissage par lesquels le striatum participe à l'apprentissage implicite d'habiletés. Rev. Neuropsychol. 12 (2002) 379-399
37. Mayr U. Spatial attention and implicit sequence learning evidence for independent learning of spatial and nonspatial sequences. J. Exp. Psychol. Learn Mem. Cognit. 22 (1996) 350-364
38. Mazzoni P., Bracewell R.M., Barash S., and Anderson R.A. Motor intention activity in the macaque's lateral intraparietal area I. Dissociation of motor plan from sensory area. J. Neurophysiol. 76 (1996) 1439-1456
39. McCann R.S., and Johnston J.C. Locus of the single-cannel bottleneck in dual-task interference. J. Exp. Psychol. Hum. Percept. Perform. 18 (1992) 471-484
40. Merriam E.P., Colby C.L., Thulborn K.R., Luna B., Olson C.R., and Sweeney J.A. Stimulus-response incompatibility activates cortex proximate to three eye fields. NeuroImage 13 (2001) 794-800
41. Meyer D.E., and Kieras D.E. A computational theory of executive cognitive processes and multiple-task performance: Part 1. Basic mechanisms. Psychol. Rev. 104 (1997) 3-65
42. Miller E.K., and Cohen J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24 (2001) 167-202
43. Mushiake H., Inase M., and Tanji J. Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. J. Neurophysiol. 66 (1991) 705-718
44. Nissen M.J., and Bullemer P. Attentional requirements of learning: evidence from performance measures. Cognit. Psychol. 19 (1987) 1-32
45. Olson I.R., Rao H., Moore K.S., Wang J., Detre J.A., and Aguirre G.K. Using perfustion fMRI to measure continuous changes in neural activity with learning. Brain Cognit. 60 (2006) 262-271
46. Passingham R.E. The frontal Lobes and Voluntary Action (1993), Oxford Psychology Series, Oxford
47. Peigneux P., Maquet P., Meulemans T., Desterbecqz A., Laureys S., Degueldre C., Delfiore G., Aerts J., Luxen A., Franck G., Van der Linden M., and Cleeremans A. Striatum forever, despite sequence learning variability: a random effect analysis of PET data. Hum. Brain Mapp. 10 (2000) 179-194
48. Rauch S.L., Savage C.R., Brown H.D., Curran T., Alpert N.M., Kendrick A., Fischman A.J., and Kosslyn S.M. A PET investigation of implicit and explicit sequence learning. Hum. Brain Mapp. 3 (1995) 271-286
49. Rauch S.L., Savage C.R., Alpert N.M., Dougherty D., Curran T., Brown H.D., Manzo P., Fischman A.J., and Jenike M.A. Probing striatal function in obsessive-compulsive disorder: a PET study of implicit sequence learning. J. Neuropsychiatry 9 (1997) 568-573
50. Rauch S.L., Whalen P.J., Savage C.R., Curran T., Kendrick A., Brown H.D., Bush G., Breiter H.C., and Rosen B.R. Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging. Hum. Brain Mapp. 5 (1997) 124-132
51. Rauch S.L., Whalen P.J., Curran T., McInerney S., Heckers S., and Savage C.R. Thalamic deactivation during early implicit sequence learning: a functional MRI study. NeuroReport 9 (1998) 865-870
52. Reed J., and Johnson P. Assessing implicit learning with indirect tests: determining what is learned about sequence structure. J. Exp. Psychol. Learn Mem. Cognit. 20 (1994) 585-594
53. Rowe J.B., and Passingham R.E. Working memory for location and time: activity in prefrontal area 46 relates to selection rather than maintenance in memory. NeuroImage 14 (2001) 77-86
54. Rowe J.B., Toni I., Josephs O., Frackowiak R.S.J., and Passingham R.E. The prefrontal cortex: response selection or maintenance within working memory?. Science 288 (2000) 1656-1660
55. Sanders A.F. Stage analysis of reaction processes. In: Stelmach G.E., and Requin J. (Eds). Tutorials in Motor Behavior (1980), North-Holland, New York 331-354
56. Schendan H.E., Searl M.M., Melrose R.J., and Stern C.E. An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 37 (2003) 1013-1025
57. Schneider W., Eschman A., and Zuccolotto A. E-Prime User's Guide (2002), Psychology Software Tools, Inc., Pittsburgh
58. Schumacher E.H., and D'Esposito M. Neural implementation of response selection in humans as revealed by localizing effects of stimulus-response compatibility on brain activation. Hum. Brain Mapp. 17 (2002) 193-201
59. Schumacher, E.H., Schwarb, H., 2008. Parallel response selection disrupts sequence learning under dual task conditions. Manuscript under review.
60. Schumacher E.H., Lauber E.J., Glass J.M., Zurbriggen E.L., Gmeindl L., Kieras D.E., and Meyer D.E. Concurrent response-selection processes in dual-task performance: evidence for adaptive executive control of task scheduling. J. Exp. Psychol. Hum. Percept. Perform. 25 (1999) 791-814
61. Schumacher E.H., Elston P.A., and D'Esposito M. Neural evidence for representation-specific response selection. J. Cognit. Neurosci. 15 (2003) 1111-1121
62. Schumacher E.H., Hendricks M.J., and D'Esposito M. Sustained involvement of a frontal-parietal network for spatial response selection with practice of a spatial choice-reaction task. Neuropsychologia 43 (2005) 1444-1455
63. Schumacher E.H., Cole M.W., and D'Esposito M. Selection and maintenance of stimulus-response rules during preparation and performance of a spatial choice-reaction task. Brain Res. 1136 (2007) 77-87
64. Schwarb H. The importance of stimulus-response rules in sequence learning (2008), School of Psychology. Masters Thesis. Georgia Institute of Technology, Atlanta, GA, USA
65. Seidler R.D., Purushotham A., Kim S.G., Ugurbil D., Willingham D.B., and Ashe J. Cerebellum activation associated with performance changes but not motor learning. Science 296 (2002) 2043-2046
66. Seitz R.J., Roland P.E., Bohm C., Greitz T., and Stone-Elander S. Motor learning in man: a positron emission tomographic study. NeuroReport 1 (1990) 57-60
67. Stark C.E.L., and Squire L.R. When zero is not zero: the problem of ambiguous baseline conditions in fMRI. Proc. Natl. Acad Sci. U.S.A. 98 (2001) 12760-12766
68. Sternberg S. The discovery of processing stages: extensions of Donders' method. Acta Psychol. 30 (1969) 276-315
69. Sternberg S. Separate modifiability, mental modules, and the use of pure and composite measures to reveal them. Acta Psychol. 106 (2001) 147-246
70. Strauss W.L., Tsuruda J.S., and Richards T.L. Partial volume effects in volume-localized phased-array proton spectroscopy of the temporal lobe. J. Magn. Reson. Imag. 5 (1995) 433-436
71. Tanji J. Sequential organization of multiple movements: involvement of cortical motor areas. Annu. Rev. Neurosci. 24 (2001) 631-651
72. van der Graaf F.H.C.E., Maguire R.P., Leenders K.L., and de Jong B.M. Cerebral activation related to implicit sequence learning in a double serial reaction time task. Brain Res. 1081 (2006) 179-190
73. Willingham D.B. Implicit motor sequence learning is not purely perceptual. Mem. Cognit. 27 (1999) 561-572
74. Willingham D.B., Nissen M.J., and Bullemer P. On the development of procedural knowledge. J. Exp. Psychol. Learn Mem. Cognit. 15 (1989) 1047-1060
75. Willingham D.B., Wells L.A., Farrell J.M., and Stemwedel M.E. Implicit motor sequence learning is represented in response locations. Mem. Cognit. 28 (2000) 366-375
76. Wise S.P., Boussaoud D., Johnson P.B., and Caminiti R. Premotor and parietal cortex: Corticocortical connectivity and combinatorial computations. Annu. Rev. Neurosci. 20 (1997) 25-42
77. Worsley K.J., and Friston K.J. Analysis of fMRI time-series revisited-again. NeuroImage 2 (1995) 173-182