Neural basis of repetition priming during mathematical cognition: Repetition suppression or repetition enhancement?

Journal of Cognitive Neuroscience

Volumn 22, Issue 4, 2010, Pages 790-805

  Salimpoor, Valorie N ^a,b   Chang, Catie ^b   Menon, Vinod ^b  

^a MCGILL UNIVERSITY   (Canada)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BEHAVIORAL RESEARCH; BRAIN REGION; BRODMANN AREA; CINGULATE GYRUS; COGNITION; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROENCEPHALOGRAM; FACILITATION; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MATHEMATICAL ANALYSIS; MEMORY; NERVE CONDUCTION; NEUROIMAGING; NORMAL HUMAN; PRECUNEUS CORTEX; PRIORITY JOURNAL; REPETITION PRIMING; RETROSPLENIAL CORTEX; STIMULUS RESPONSE; TASK PERFORMANCE; WORD RECOGNITION;

ADOLESCENT; ADULT; ASSOCIATION LEARNING; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MATHEMATICS; OXYGEN; REACTION TIME; RECOGNITION (PSYCHOLOGY); REPRESSION; YOUNG ADULT;

EID: 77649224937     PISSN: 0898929X     EISSN: 15308898     Source Type: Journal    
DOI: 10.1162/jocn.2009.21234     Document Type: Article

References (104)

1. Aizawa, H., Inase, M., Mushiake, H., Shima, K., & Tanji, J. (1991). Reorganization of activity in the supplementary motor area associated with motor learning and functional recovery. Experimental Brain Research, 84, 668-671.
2. Ansari, D. (2008). Effects of development and enculturation on number representation in the brain. Nature Reviews Neuroscience, 9, 278-291.
3. Barnea-Goraly, N., Eliez, S., Menon, V., Bammer, R., & Reiss, A. L. (2005). Arithmetic ability and parietal alterations: A diffusion tensor imaging study in velocardiofacial syndrome. Brain Research, Cognitive Brain Research, 25, 735-740.
4. Benton, A. L. (1987). Mathematical disability and the Gerstmann syndrome. In G. Deloche & X. Seron (Eds.), Mathematical disabilities: A cognitive neuropsychological perspective. New Jersey: Lawrence Erlbaum.
5. Bergerbest, D., Ghahremani, D. G., & Gabrieli, J. D. (2004). Neural correlates of auditory repetition priming: Reduced fMRI activation in the auditory cortex. Journal of Cognitive Neuroscience, 16, 966-977.
6. Blaxton, T. A., Zeffiro, T. A., Gabrieli, J. D., Bookheimer, S. Y., Carrillo, M. C., Theodore, W. H., et al. (1996). Functional mapping of human learning: A positron emission tomography activation study of eyeblink conditioning. Journal of Neuroscience, 16, 4032-4040.
7. Blondin, F., & Lepage, M. (2005). Decrease and increase in brain activity during visual perceptual priming: An fMRI study on similar but perceptually different complex visual scenes. Neuropsychologia, 43, 1887-1900.
8. Buckner, R. L., & Koutstaal, W. (1998). Functional neuroimaging studies of encoding, priming, and explicit memory retrieval. Proceedings of the National Academy of Sciences, U.S.A., 95, 891-898.
9. Buckner, R. L., Koutstaal, W., Schacter, D. L., Wagner, A. D., & Rosen, B. R. (1998). Functional-anatomic study of episodic retrieval using fMRI: I. Retrieval effort versus retrieval success. Neuroimage, 7, 151-162.
10. Buckner, R. L., Petersen, S. E., Ojemann, J. G., Miezin, F. M., Squire, L. R., & Raichle, M. E. (1995). Functional anatomical studies of explicit and implicit memory retrieval tasks. Journal of Neuroscience, 15, 12-29.
11. Bunzeck, N., Schutze, H., & Duzel, E. (2006). Category-specific organization of prefrontal response-facilitation during priming. Neuropsychologia, 44, 1765-1776.
12. Busch, N. A., Groh-Bordin, C., Zimmer, H. D., & Herrmann, C. S. (2008). Modes of memory: Early electrophysiological markers of repetition suppression and recognition enhancement predict behavioral performance. Psychophysiology, 45, 25-35.
13. Cappelletti, M., Barth, H., Fregni, F., Spelke, E., & Pascual-Leone, A. (2007). rTMS over the intraparietal sulcus disrupts numerosity processing. Experimental Brain Research, 179, 631-642.
14. Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: A review of its functional anatomy and behavioral correlates. Brain, 129, 564-583.
15. Chein, J. M., & Schneider, W. (2005). Neuroimaging studies of practice-related change: fMRI and meta-analytic evidence of a domain-general control network for learning. Brain Research, Cognitive Brain Research, 25, 607-623.
16. Cohen, N. J., Poldrack, R. A., & Eichenbaum, H. (1998). Memory for items and memory for relations in the procedural/declarative memory framework. Memory, 5, 131-178.
17. Danker, J. F., & Anderson, J. R. (2007). The roles of prefrontal and posterior parietal cortex in algebra problem solving: A case of using cognitive modeling to inform neuroimaging data. Neuroimage, 35, 1365-1377.
18. Davachi, L., Mitchell, J. P., & Wagner, A. D. (2003). Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories. Proceedings of the National Academy of Sciences, U.S.A., 100, 2157-2162.
19. Dehaene, S., Spelke, E., Pinel, P., Stanescu, R., & Tsivkin, S. (1999). Sources of mathematical thinking: Behavioral and brain-imaging evidence. Science, 284, 970-974.
20. Delazer, M., Benke, T., Trieb, T., Schocke, M., & Ischebeck, A. (2006). Isolated numerical skills in posterior cortical atrophy - An fMRI study. Neuropsychologia, 44, 1909-1913.
21. Delazer, M., Domahs, F., Bartha, L., Brenneis, C., Lochy, A., Trieb, T., et al. (2003). Learning complex arithmetic - An fMRI study. Brain Research, Cognitive Brain Research, 18, 76-88.
22. Delazer, M., Ischebeck, A., Domahs, F., Zamarian, L., Koppelstaetter, F., Siedentopf, C. M., et al. (2005). Learning by strategies and learning by drill-evidence from an fMRI study. Neuroimage, 25, 838-849.
23. Delazer, M., Karner, E., Zamarian, L., Donnemiller, E., & Benke, T. (2006). Number processing in posterior cortical atrophy - A neuropsychological case study. Neuropsychologia, 44, 36-51.
24. Demb, J. B., Desmond, J. E., Wagner, A. D., Vaidya, C. J., Glover, G. H., & Gabrieli, J. D. (1995). Semantic encoding and retrieval in the left inferior prefrontal cortex: A functional MRI study of task difficulty and process specificity. Journal of Neuroscience, 15, 5870-5878.
25. Desimone, R. (1996). Neural mechanisms for visual memory and their role in attention. Proceedings of the National Academy of Sciences, U.S.A., 93, 13494-13499.
26. Dobbins, l. G., Schnyer, D. M., Verfaellie, M., & Schacter, D. L. (2004). Cortical activity reductions during repetition priming can result from rapid response learning. Nature, 428, 316-319.
27. Doniger, G. M., Foxe, J. J., Schroeder, C. E., Murray, M. M., Higgins, B. A., & Javitt, D. C. (2001). Visual perceptual learning in human object recognition areas: A repetition priming study using high-density electrical mapping. Neuroimage, 13, 305-313.
28. Duvernoy, H. M., Bourgouin, P., Cabanis, E. A., & Cattin, F. (1999). The human brain: Functional anatomy, vascularization and serial sections with MRI. New York: Springer.
29. Eger, E., Henson, R. N., Driver, J., & Dolan, R. J. (2004). BOLD repetition decreases in object-responsive ventral visual areas depend on spatial attention. Journal of Neurophysiology, 92, 1241-1247.
30. Eger, E., Schweinberger, S. R., Dolan, R. J., & Henson, R. N. (2005). Familiarity enhances invariance of face representations in human ventral visual cortex: fMRI evidence. Neuroimage, 26, 1128-1139.
31. Fiebach, C. J., Gruber, T., & Supp, G. G. (2005). Neuronal mechanisms of repetition priming in occipitotemporal cortex: Spatiotemporal evidence from functional magnetic resonance imaging and electroencephalography. Journal of Neuroscience, 25, 3414-3422.
32. Friston, K. J., Buechel, C., Fink, G. R., Morris, J., Rolls, E., & Dolan, R. J. (1997). Psychophysiological and modulatory interactions in neuroimaging. Neuroimage, 6, 218-229.
33. Gagnepain, P., Chetelat, G., Landeau, B., Dayan, J., Eustache, F., & Lebreton, K. (2008). Spoken word memory traces within the human auditory cortex revealed by repetition priming and functional magnetic resonance imaging. Journal of Neuroscience, 28, 5281-5289.
34. Ganel, T., Gonzalez, C. L., Valyear, K. F., Culham, J. C., Goodale, M. A., & Kohler, S. (2006). The relationship between fMRI adaptation and repetition priming. Neuroimage, 32, 1432-1440.
35. Gilaie-Dotan, S., Nir, Y., & Malach, R. (2008). Regionally-specific adaptation dynamics in human object areas. Neuroimage, 39, 1926-1937.
36. Giovanello, K. S., Schnyer, D. M., & Verfaellie, M. (2004). A critical role for the anterior hippocampus in relational memory: Evidence from an fMRI study comparing associative and item recognition. Hippocampus, 14, 5-8.
37. Grill-Spector, K., Kushnir, T., Edelman, S., Avidan, G., Itzchak, Y., & Malach, R. (1999). Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron, 24, 187-203.
38. Grill-Spector, K., & Malach, R. (2001). fMR-adaptation: A tool for studying the functional properties of human cortical neurons. Acta Psychologica, 107, 293-321.
39. Gruber, O., Indefrey, P., Steinmetz, H., & Kleinschmidt, A. (2001). Dissociating neural correlates of cognitive components in mental calculation. Cerebral Cortex, 11, 350-359.
40. Gupta, P., & Cohen, N. J. (1990). Theoretical and computational analysis of skill learning, repetition priming, and procedural memory. Psychological Review, 109, 401-448.
41. Habeck, C., Hilton, H. J., Zarahn, E., Brown, T., & Stern, Y. (2006). An event-related fMRI study of the neural networks underlying repetition suppression and reaction time priming in implicit visual memory. Brain Research, 1075, 133-141.
42. Hagoort, P. (1997). Semantic priming in Broca's aphasics at a short SOA: No support for an automatic access deficit. Brain and Language, 56, 287-300.
43. Hamann, S. B., & Squire, L. R. (1996). Level-of-processing effects in word-completion priming: A neuropsychological study. Journal of Experimental Psychology: Learning, Memory, and Cognition, 22, 933-947.
44. Hatanaka, N., Tokuno, H., Hamada, I., Inase, M., Ito, Y., Imanishi, M., et al. (2003). Thalamacotical and intracortical connections of monkey cingulate motor areas. Journal of Comparative Neurology, 462, 121-138.
45. Henson, R., & Mouchlianitis, E. (2007). Effect of spatial attention on stimulus-specific haemodynamic repetition effects. Neuroimage, 35, 1317-1329.
46. Henson, R., Shallice, T., & Dolan, R. (2000). Neuroimaging evidence for dissociable forms of repetition priming. Science, 287, 1269-1272.
47. Henson, R. N., & Rugg, M. D. (2003). Neural response suppression, haemodynamic repetition effects, and behavioural priming. Neuropsychologia, 41, 263-270.
48. Henson, R. N. (2003). Neuroimaging studies of priming. Progress in Neurobiology, 70, 53-81.
49. Henson, R. N., Hornberger, M., & Rugg, M. D. (2005). Further dissociating the processes involved in recognition memory: An fMRI study. Journal of Cognitive Neuroscience, 17, 1058-1073.
50. Henson, R. N., Shallice, T., Gorno-Tempini, M. L., & Dolan, R. J. (2002). Face repetition effects in implicit and explicit memory tests as measured by fMRI. Cerebral Cortex, 12, 178-186.
51. Hill, N. M., & Schneider, W. (2006). Brain changes in the development of expertise: Neurological evidence on skill-based adaptations. In K. A. Ericsson, N. Charness, P. Feltovich, & R. Hoffman (Eds.), The Cambridge handbook of expertise and expert performance (pp. 653-682). Cambridge, MA: Cambridge University Press.
52. Horner, A. J., & Henson, R. N. (2008). Priming, response learning and repetition suppression. Neuropsychologia, 46, 1979-1991.
53. Houde, O., & Tzourio-Mazoyer, N. (2003). Neural foundations of logical and mathematical cognition. Nature Reviews Neuroscience, 4, 507-514.
54. Hubbard, E. M., Piazza, M., Pinel, P., & Dehaene, S. (2005). Interactions between number and space in parietal cortex. Nature Reviews Neuroscience, 6, 435-448.
55. Kirwan, C. B., & Stark, C. E. (2004). Medial temporal lobe activation during encoding and retrieval of novel face-name pairs. Hippocampus, 14, 919-930.
56. Koutstaal, W., Wagner, A. D., Rotte, M., Maril, A., Buckner, R. L., & Schacter, D. L. (2001). Perceptual specificity in visual object priming: Functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex. Neuropsychologia, 39, 184-199.
57. Lee, D., & Quessy, S. (2003). Activity in the supplementary motor area related to learning and performance during a sequential visuomotor task. Journal of Neurophysiology, 89, 1039-1056.
58. Levin, H. S., Scheller, J., Rickard, T., Graftman, J., Martinkowski, K., Winslow, M., et al. (1996). Dyscalculia and dyslexia after right hemisphere injury in infancy. Archives of Neurology, 53, 88-96.
59. Li, L. (1993). The representation of stimulus familiarity in anterior inferior temporal cortex. Journal of Neurophysiology, 69, 1918-1929.
60. Lin, C. Y., & Ryan, L. (2007). Repetition priming without identification of the primes: Evidence for a component process view of priming. Neuroimage, 38, 589-603.
61. Logan, G. D. (1990). Repetition priming and automaticity: Common underlying mechanisms? Cognitive Psychology, 22, 1-35.
62. Lustig, C., & Buckner, R. L. (2004). Preserved neural correlates of priming in old age and dementia. Neuron, 42, 865-875.
63. Maccotta, L., & Buckner, R. L. (2004). Evidence for neural effects of repetition that directly correlate with behavioral priming. Journal of Cognitive Neuroscience, 16, 1625-1632.
64. Martin, R. C., & Cheng, Y. (2006). Selection demands versus association strength in the verb generation task. Psychonomic Bulletin & Review, 13, 396-401.
65. McMahon, D. B. T., & Olson, C. R. (2007). Repetition suppression in monkey inferotemporal cortex: Relation to behavioral priming. Journal of Neurophysiology, 97, 3532-3543.
66. Menon, V., & Levitin, D. J. (2005). The rewards of music listening: Response and physiological connectivity of the mesolimbic system. Neuroimage, 28, 175-184.
67. Menon, V., Mackenzie, K., Rivera, S. M., & Reiss, A. L. (2002). Prefrontal cortex involvement in processing incorrect arithmetic equations: Evidence from event-related fMRI. Human Brain Mapping, 16, 119-130.
68. Menon, V., Rivera, S. M., White, C. D., Eliez, S., Glover, G. H., & Reiss, A. L. (2000). Functional optimization of arithmetic processing in perfect performers. Brain Research, Cognitive Brain Research, 9, 343-345.
69. Menon, V., Rivera, S. M., White, C. D., Glover, G. H., & Reiss, A. L. (2000). Dissociating prefrontal and parietal cortex activation during arithmetic processing. Neuroimage, 12, 357-365.
70. Miller, E. K., Li, L., & Desimone, R. (1991). A neural mechanism for working and recognition memory in inferior temporal cortex. Science, 254, 5036.
71. Morton, J. (1969). The interaction of information in word recognition. Psychological Review, 76 165-178.
72. Naccache, L., & Dehaene, S. (2001). The priming method: Imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. Cerebral Cortex, 11, 966-974.
73. Orfanidou, E., Marslen-Wilson, W. D., & Davis, M. H. (2006). Neural response suppression predicts repetition priming of spoken words and pseudowords. Journal of Cognitive Neuroscience, 18, 1237-1252.
74. Parvizi, J., Van hoesen, G. W., Buckwalter, J., & Damasio, A. (2006). Neural connections of the posteriomedia cortex in the macaque. Proceedings of the National Academy of Sciences, U.S.A., 103, 1563-1568.
75. Paz, R., Natan, C., Boraud, T., Bergman, H., & Vaadia, E. (2005). Emerging patterns of neuronal responses in supplementary and primary motor areas during sensorimotor adaptation. Journal of Neuroscience, 25, 10941-10951.
76. Qin, Y., Sohn, M. H., Anderson, J. R., Stenger, V. A., Fissell, K., Goode, A., et al. (2003). Predicting the practice effects on the blood oxygenation level-dependent (BOLD) function of fMRI in a symbolic manipulation task. Proceedings of the National Academy of Sciences, U.S.A., 100, 4951-4956.
77. Raichle, M. E., Fiez, J. A., Videen, T. O., MacLeod, A. M., Pardo, J. V., Fox, P. T., et al. (1994). Practice-related changes in human brain functional anatomy during nonmotor learning. Cerebral Cortex, 4, 8-26.
78. Rainer, G., & Miller, E. K. (2000). Effects of visual experience on the representation of objects in the prefrontal cortex. Neuron, 27, 8-10.
79. Ranganath, C., Yonelinas, A. P., Cohen, M. X., Dy, C. J., Tom, S. M., & D'Esposito, M. (2004). Dissociable correlates of recollection and familiarity within the medial temporal lobes. Neuropsychologia, 42, 2-13.
80. Rickard, T., Romero, S. G., Basso, G., Wharton, C. M., Filtman, S., & Grafman, J. (2000). The calculating brain: An fMRI study. Neuropsychologia, 38, 325-335.
81. Rivera, S. M., Menon, V., White, C. D., Glaser, B., & Reiss, A. L. (2002). Functional brain activation during arithmetic processing in females with fragile X Syndrome is related to FMR1 protein expression. Human Brain Mapping, 16, 206-218.
82. Roediger, H. L. (2003). Rethinking implicit memory. In J. S. Bowers & C. J. Marsolek (Eds.), Rethinking implicit memory. Oxford University Press.
83. Ryan, L., & Schnyer, D. M. (2007). Regional specificity of format specific priming effects in word reading using functional magnetic resonance imaging. Cerebral Cortex, 17, 982-992.
84. Sayres, R., & Grill-Spector, K. (2006). Object-selective cortex exhibits performance-independent repetition suppression. Journal of Neurophysiology, 95, 995-1007.
85. Scarborough, D. L., Cortese, C., & Scarborough, H. (1977). Frequency and repetition effects in lexical memory. Journal of Experimental Psychology: Human Perception and Performance, 3, 1-17.
86. Schacter, D. L., Wig, G. S., & Stevens, W. D. (2007). Reductions in cortical activity during priming. Current Opinion in Neurobiology, 17, 171-176.
87. Schnyer, D. M., Dobbins, I. G., Nicholls, L., Schacter, D. L., & Verfaellie, M. (2006). Rapid response learning in amnesia: Delineating associative learning components in repetition priming. Neuropsychologia, 44, 140-149.
88. Sciama, S. C., Semenza, C., & Butterworth, B. (1999). Repetition priming in simple addition depends on surface form and typicality. Memory & Cognition, 27, 116-127.
89. Sohn, M. H., Goode, A., Stenger, V. A., Carter, C. S., & Anderson, J. R. (2003). Competition and representation during memory retrieval: Roles of the prefrontal cortex and the posterior parietal cortex. Proceedings of the National Academy of Sciences, U.S.A., 100, 7412-7417.
90. Speelman, C. P., Simpson, T. A., & Kirsner, K. (2002). The unbearable lightness of priming. Acta Psychologica, 111, 191-204.
91. Suzuki, W. A. (2008). Associative learning signals in the brain. Progress in Brain Research, 169, 305-320.
92. Takayama, Y., Sugishita, M., Akiguchi, I., & Kimura, J. (1994). Isolated acalculia due to left parietal lesion. Archives of Neurology, 51, 286-291.
93. Thompson-Schill, S. L., & Botvinick, M. M. (2006). Resolving conflict: A response to Martin and Cheng (2006). Psychonomic Bulletin & Review, 13, 402-408; discussion 409-411.
94. Turk-Browne, N. B., Yi, D. J., & Chun, M. M. (2006). Linking implicit and explicit memory: Common encoding factors and shared representations. Neuron, 49, 917-927.
95. Van essen, D. C., Anderson, C. H., & Felleman, D. J. (1992). Information processing in the primate visual system: An integrated systems perspective. Science, 255, 419-423.
96. Vincent, J. L., Snyder, A. Z., Fox, M. D., Shannon, B. J., Andrews, J. R., Raichle, M. E., et al. (2006). Coherent spontaneous activity identifies a hippocampal-parietal memory network. Journal of Neurophysiology, 96, 3517-3531.
97. Vogt, B. A., Berger, G. R., & Derbyshire, S. W. (2003). Structural and functional dichotomy of human midcingulate cortex. European Journal of Neuroscience.
98. Vogt, B. A., Hof, P. R., & Vogt, L. J. (2004). Cingulate gyrus. In G. Paxinos & J. K. Mai (Eds.), The human nervous system (pp. 915-949). San Diego: Elsevier.
99. Wagner, A. D., Gabrieli, J. D., & Verfaellie, M. (1997). Dissociations between familiarity processes in explicit recognition and implicit perceptual memory. Journal of Experimental Psychology: Learning, Memory, and Cognition, 23, 305-323.
100. Wagner, A. D., Pare-Blagoev, E. J., Clark, J., & Poldrack, R. A. (2001). Recovering meaning: Left prefrontal cortex guides controlled semantic retrieval. Neuron, 31, 329-338.
101. Wig, G. S., Grafton, S. T., Demos, K. E., & Kelley, W. M. (2005). Reductions in neural activity underlie behavioral components of repetition priming. Nature Neuroscience, 8, 1228-1233.
102. Wiggs, C. L., & Martin, A. (1998). Properties and mechanisms of perceptual priming. Current Opinion in Neurobiology, 8, 227-233.
103. Zago, L., Fenske, M. J., Aminoff, E., & Bar, M. (2005). The rise and fall of priming: How visual exposure shapes cortical representations of objects. Cerebral Cortex, 15, 1655-1665.
104. Zago, L., & Tzourio-Mazoyer, N. (2002). Distinguishing visuospatial working memory and complex mental calculation areas within the parietal lobes. Neuroscience Letters, 331, 45-49.