Combining fMRI and behavioral measures to examine the process of human learning

Neurobiology of Learning and Memory

Volumn 109, Issue , 2014, Pages 193-206

  Karuza, Elisabeth A ^a   Emberson, Lauren L ^a   Aslin, Richard N ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Behavioral measures; Cognitive neuroscience; FMRI; Learning; Outcome measures; Process; Time course

Indexed keywords

BEHAVIORAL MEASURES; COGNITIVE NEUROSCIENCE; FMRI; LEARNING; OUTCOME MEASURES; PROCESS; TIME-COURSE;

BRAIN; BRAIN MAPPING; HUMANS; LEARNING; MAGNETIC RESONANCE IMAGING; PSYCHOMOTOR PERFORMANCE; RESEARCH DESIGN;

EID: 84894274162     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.09.012     Document Type: Review

References (93)

1. Abla D., Katahira K., Okanoya K. Online assessment of statistical learning by event-related potentials. Journal of Cognitive Neuroscience 2008, 20:952-964.
2. Bayley P., O'Reilly R., Curran T., Squire L. New semantic learning in patients with large medial temporal lobe lesions. Hippocampus 2008, 18:575-583.
3. Behrens T.E., Hunt L.T., Woolrich M.W., Rushworth M.F. Associative learning of social value. Nature 2008, 456:245-249.
4. Behrens T.E., Woolrich M.W., Walton M.E., Rushworth M.F. Learning the value of information in an uncertain world. Nature Neuroscience 2007, 10:1214-1221.
5. Belliveau J., Kennedy D., McKinstry R., Buchbinder B., Weisskoff R., Cohen M., et al. Functional mapping of the human visual cortex by magnetic resonance imaging. Science 1991, 254:716-719.
6. Caramazza A., Badecker W. Clinical syndromes are not God's gift to cognitive neuropsychology : A reply to a rebuttal to an answer to a response to the case against syndrome-based research. Brain & Cognition 1991, 16:211-227.
7. Cunillera T., Càmara E., Toro J.M., Marco-Pallares J., Sebastián-Galles N., Oritz H., et al. Time course and functional neuroanatomy of speech segmentation in adults. Neuroimage 2009, 48:541-553.
8. Daniel R., Pollmann S. Striatal activations signal prediction errors on confidence in the absence of external feedback. Neuroimage 2012, 59:3457-3467.
9. Dayan P., Daw N.D. Decision theory, reinforcement learning and the brain. Cognitive, Affective, & Behavioral Neuroscience 2008, 8:429-453.
10. Dienes Z., Broadbent D., Berry D. Implicit and explicit knowledge bases in artificial grammar learning. Journal of Experimental Psychology: Learning, Memory and Cognition 1991, 17:875-887.
11. den Ouden H.E.M., Daunizeau J., Roiser J., Friston K., Stephan K. Striatal prediction error modulates cortical coupling. Journal of Neuroscience 2010, 30:3210-3219.
12. den Ouden H.E.M., Friston K.J., Daw N., McIntosh A.R., Stephan K.E. A dual-role for prediction error in associative learning. Cerebral Cortex 2009, 19:1175-1851.
13. Dolan R.J., Fletcher P.F. Encoding and retrieval in the human medial temporal lobes: An empirical investigation using functional magnetic resonance imaging. Hippocampus 1999, 9:25-34.
14. Doyon J., Bellec P., Amsel R., Penhune V.B., Monchi O., Benali H. Contributions of the basal ganglia and functionally related brain structures to motor learning. Behavioral and Brain Research 2009, 199:61-75.
15. Eichenbaum H., Cohen N. From conditioning to conscious recollection: Memory systems of the brain 2001, Oxford University Press, USA.
16. Elman J.L. Finding structure in time. Cognitive Science 1990, 14:179-211.
17. Emberson L.L., Amso D. Learning to sample: Eye tracking and fMRI indices of changes in object perception. Journal of Cognitive Neuroscience 2012, 24:2030-2042.
18. Fiser J., Aslin R.N. Statistical learning of new visual feature combinations by infants. Proceedings of the National Academy of Sciences 2002, 99:15822-15826.
19. Fiser J., Aslin R.N. Encoding multi-element scenes: Statistical learning of visual feature hierarchies. Journal of Experimental Psychology: General 2005, 134:521-537.
20. Fiser J., Scholl B.J., Aslin R.N. Perceived object trajectories during occlusion constrain visual statistical learning. Psychological Bulletin and Review 2007, 14:173-178.
21. Forkstam C., Hagoort P., Fernandez G., Ingvar M., Petersson K.M. Neural correlates of artificial syntactic structure classification. Neuroimage 2006, 32:956-967.
22. Forkstam C., Petersson K.M. Towards an explicit account of implicit learning. Current Opinion in Neurobiology 2005, 18:435-441.
23. Furl N., Kumar S., Alter K., Durrant S., Shawe-Taylor J., Griffiths T. Neural prediction of higher-order auditory sequence statistics. Neuroimage 2011, 54:2267-2277.
24. Gebhart A.L., Newport E.L., Aslin R.N. Statistical learning of adjacent and non-adjacent dependencies among nonlinguistic sounds. Psychonomic Bulletin & Review 2009, 16:486-490.
25. Gershman S.J., Niv Y. Learning latent structure: Carving nature at its joints. Current Opinion in Neurobiology 2010, 20:251-256.
26. Gheysen F., Van Opstal F., Roggeman C., Van Waelvelde H., Fias W. The neural basis of implicit perceptual sequence learning. Frontiers in Human Neuroscience 2011, 5:1-12.
27. Habib R., Nyberg L., Tulving E. Hemispheric asymmetries of memory: The HERA model revised. Trends in Cognitive Sciences 2003, 7:241-245.
28. Haykin S. Neural networks: A comprehensive foundation 1998, Prentice-Hall, Upper Saddle River, NJ. 2nd ed.
29. Hunt R.H., Aslin R.N. Statistical learning in a serial reaction time task: Simultaneous extraction of multiple statistics. Journal of Experimental Psychology: General 2001, 130:658-680.
30. Johnson S., Slemmer J., Amso D. Where infants look determines how they see: Eye movements and object perception performance in 3-month-olds. Infancy 2004, 6:185-201.
31. Karni A., Meyer G., Jezzard P., Adams M.M., Turner R., Ungerleider L.G. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 1995, 377:155-158.
32. Karuza E., Newport E., Aslin R., Starling S., Tivarus M., Bavelier D. Neural correlates of statistical learning in a word segmentation task: An fMRI study. Brain and Language: Special Issue 2013, (in press).
33. Kidd C., Piantadosi S., Aslin R. The goldilocks effect: Human infants allocate attention to visual sequences that are neither too simple nor too complex. PLoS ONE 2012, 7:e36399.
34. Kirkham N., Slemmer J., Johnson S. Visual statistical learning in infancy: Evidence for a domain general learning mechanism. Cognition 2002, 83:B35-B42.
35. Knowlton B.J., Squire L.R. Artificial grammar learning depends on implicit acquisition of both abstract and exemplar-specific information. Journal of Experimental Psychology: Learning and Memory Cognition 1996, 22:169-181.
36. Kruschke J. Locally Bayesian learning with applications to retrospective revaluation and highlighting. Psychological Review 2006, 113:677-698.
37. Lehéricy S., Benali H., Van de Moortele P.F., Pélégrini-Issac M., Waechter T., Ugurbil K., et al. Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proceedings of the National Academy of Sciences 2005, 102:12566-12571.
38. Lieberman M.D., Chang G.Y., Chiao J., Bookheimer S.Y., Knowlton B.J. An event-related fMRI study of artificial grammar learning in a balanced chunk strength design. Journal of Cognitive Neuroscience 2004, 16:427-438.
39. Logothetis N.K., Wandell B.A. Interpreting the bold signal. Annual Review of Psychology 2004, 66:735-769.
40. McNealy K., Mazziotta J.C., Dapretto M. Cracking the language code: Neural mechanisms underlying speech parsing. Journal of Neuroscience 2006, 26:7629-7639.
41. McNealy K., Mazziotta J.C., Dapretto M. The neural basis of speech parsing in children and adults. Developmental Science 2010, 13:385-406.
42. Miller R., Barnet R.C., Grahame N.J. Assessment of the Rescorla-Wagner model. Psychological Bulletin 1995, 117:363-386.
43. Muehlhan M., Lueken U., Wittchen H.-U., Kirschbaum C. The scanner as a stressor: Evidence from subjective and neuroendocrine stress parameters in the time course of an functional magnetic resonance imaging session. International Journal of Psychophysiology 2011, 79:118-126.
44. Newport E.L., Aslin R.N. Learning at a distance I. Statistical learning of non-adjacent dependencies. Cognitive Psychology 2004, 48:127-162.
45. Nissen M.J., Bullemer P. Attentional requirements of learning: Evidence from performance measures. Cognitive Psychology 1987, 19:1-32.
46. Norman K., O'Reilly R. Modeling hippocampal and neocortical contributions to recognition memory: A complementary-learning-systems approach. Psychological Review 2003, 110:611-645.
47. Ogawa S., Tank D.W., Menon R., Ellermann J.M., Kim S.-G., Merkle H., et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proceedings of the National Academy of Sciences 1992, 89:5951-5955.
48. Opitz B., Rinne T., Mecklinger A., von Cramon D.Y., Schröger E. Differential contribution of frontal and temporal cortices to auditory change detection: fMRI and ERP results. Neuroimage 2002, 15:167-174.
49. Orban, G., Aslin, R.N., Fiser J. and Lengyel, M., Occam's razor at work: The dynamics of visual chunk learning, in preparation.
50. Pavlov I.P. Conditioned reflexes: An investigation of the physiological activity of the cerebral cortex. Translated and Edited by G. V. Anrep 1927, Oxford University Press, London.
51. Petersson K.-M., Folia V., Hagoort P. What artificial grammar learning reveals about the neurobiology of syntax. Brain and Language 2012, 120:83-95.
52. Petersson K.M., Forkstam C., Ingvar M. Artificial syntactic violations activate Broca's region. Cognitive Science 2004, 28:383-407.
53. Poldrack R., Clark J., Pare-Blagoev E., Shohamy D., Moyano J., Myers C., et al. Interactive memory systems in the human brain. Nature 2001, 414:546-550.
54. Poldrack R., Prabhakaran V., Seger C., Gabrieli J. Striatal activation during acquisition of a cognitive skill. Neuropsychology 1999, 13:564-574.
55. Rauch S.L., Whalen P.J., Savage C.R., Curran T., Kendrick A., Brown H.D., et al. Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging. Human Brain Mapping 1997, 5:124-132.
56. Reber A.S. Implicit learning of artificial grammars. Journal of Verbal Learning and Verbal Behavior 1967, 6:855-863.
57. Reber A.S. Implicit learning and tacit knowledge: An essay on the cognitive unconscious 1993, Oxford University Press, New York.
58. Reber A.S., Walkenfeld F.F., Henstad R. Implicit and explicit learning: individual differences and IQ. Journal of Experimental Psychology: Learning, Memory and Cognition 1991, 17:888-896.
59. Reeder, P.A., Aslin, R.N., Newport, E.L. and Bavelier, D., Learning-rate differences in expert players of first-person-shooter video games, in preparation.
60. Rescorla R., Wagner A. A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. Classical conditioning II: Current research and theory 1972, 64-99. Appleton-Century-Crofts, New York. A. Black, W. Prokasy (Eds.).
61. Rescorla R.A. Behavioral studies of Pavlovian conditioning. Annual Review of Neuroscience 1988, 11:329-352.
62. Ross R., Brown T., Stern C. The retrieval of learned sequences engages the hippocampus: Evidence from fMRI. Hippocampus 2009, 19:790-799.
63. Saffran J., Aslin R., Newport E. Statistical learning by 8-month-old infants. Science 1996, 274:1926-1928.
64. Saffran J.R., Newport E.L., Aslin R.N. Word segmentation: The role of distributional cues. Journal of Memory and Language 1996, 35:606-621.
65. Sakai K., Hikosaka O.K., Miyauchi S., Takino R., Sasaki Y., Putz B. Transition of brain activation from frontal to parietal areas in visuomotor sequence learning. Journal of Neuroscience 1998, 18:1827-1840.
66. Sakamoto Y., Jones M., Love B.C. Putting the psychology back into psychological models: Mechanistic versus rational approaches. Memory & Cognition 2008, 36:1057-1065.
67. Schendan H.E., Searl M.M., Melrose R.J., Stern C.E. An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 2003, 37:1013-1025.
68. Schultz W., Dayan P., Montague P.R. A neural substrate for prediction and reward. Science 1997, 275:1593-1599.
69. Seger C.A., Cincotta C.M. Dynamics of frontal, striatal, and hippocampal systems in rule learning. Cerebral Cortex 2006, 16:1546-1555.
70. Seger C.A., Prabhakaran V., Poldrack R.A., Gabrieli J.D.E. Neural activity differs between explicit and implicit learning of artificial grammar strings: An fMRI study. Psychobiology 2000, 28:283-292.
71. Shadmehr R., Holcomb H.H. Neural correlates of motor memory consolidation. Science 1997, 277:821-825.
72. Shanks D.R., St.John M.F. Characteristics of dissociable human learning systems. Behavioral and Brain Sciences 1994, 17:367-447.
73. Shohamy D., Wagner A. Integrating memories in the human brain: Hippocampal-midbrain encoding of overlapping events. Neuron 2008, 60:378-389.
74. Skinner B.F. The behavior of organisms: An experimental analysis 1938, Appleton Century, New York.
75. Skosnik P.D., Mirza F., Gitelman D.R., Parrish T.B., Mesulam M.-M., Reber P.J. Neural correlates of artificial grammar learning. Neuroimage 2002, 17:1306-1314.
76. Sutton R.S. Learning to predict by the methods of temporal differences. Machine Learning 1998, 3:9-44.
77. Thomas K.M., Hunt R.H., Vizueta N., Sommer T., Durston S., Yang Y., et al. Evidence of developmental differences in implicit sequence learning: an fMRI study of children and adults. Journal of Cognitive Neuroscience 2004, 16:1339-1351.
78. Thorndike E.L. Animal intelligence: Experimental studies 1911, Macmillan, New York.
79. Thorndike E.L. Human learning 1931, Century Co., New York.
80. Tolman E.C. Purposive behavior in animals and men 1951, University of California Press, Berkeley, CA.
81. Turk-Browne N., Jungé J., Scholl B. The automaticity of visual statistical learning. Journal of Experimental Psychology: General 2005, 134:552-563.
82. Turk-Browne N., Scholl B., Chun M., Johnson M.K. Neural evidence of statistical learning: Efficient detection of visual regularities without awareness. Journal of Cognitive Neuroscience 2009, 21:1934-1945.
83. Turk-Browne N.B., Scholl B.J., Johnson M.K., Chun M.M. Implicit perceptual anticipation triggered by statistical learning. Journal of Neuroscience 2010, 30:11177-11187.
84. van der Graaf F.H.C.E., Maguire R.P., Leenders K.L., de Jong B.M. Cerebral activation related to implicit sequence learning in a double serial reaction time task. Brain Research 2006, 1081:179-190.
85. Vaughn K.E., Rawson K.A. Diagnosing criterion level effects on memory: What aspects of memory are enhanced by repeated retrieval?. Psychological Science 2011, 22:1127-1131.
86. Waelti P., Dickinson A., Schultz W. Dopamine responses comply with basic assumptions of formal learning theory. Nature 2001, 412:43-48.
87. Willingham D.B., Salidis J., Gabrieli J.D. Direct comparison of neural systems mediating conscious and unconscious skill learning. Journal of Neurophysiology 2002, 88:1451-1460.
88. Wörgötter F., Porr B. Temporal sequence learning, prediction, and control: A review of different models and their relation to biological mechanisms. Neural Computation 2005, 17:245-319.
89. Yang J., Li P. Brain networks of explicit and implicit learning. PLoS ONE 2012, 7:e42993.
90. Yarkoni T., Barch D.M., Gray J.R., Conturo T.E., Braver T.S. BOLD correlates of trial-by-trial response time variability in gray and white matter: A multi- study fMRI analysis. PLoS ONE 2009, 4:e4257.
91. Zevin J., Yang J., Skipper J., McCandliss B. Domain general change detection accounts for "dishabituation" effects in temporal-parietal regions in functional magnetic resonance imaging studies of speech perception. Journal of Neuroscience 2010, 30:1110-1117.
92. Zhao J., Ngo N., McKendrick R., Turk-Browne N.B. Mutual interference between statistical summary perception and statistical learning. Psychological Science 2011, 22:1212-1219.
93. Zurif E., Swinney D., Fodor J.A. An evaluation of assumptions underlying the single-patient-only position in neuropsychological research: A reply. Brain and Cognition 1991, 16:198-210.