Repetition Priming Influences Distinct Brain Systems: Evidence From Task-Evoked Data and Resting-State Correlations
Open accessAbstract
Behavioral dissociations suggest that a single experience can separately influence multiple processing components. Here we used a repetition priming functional magnetic resonance imaging paradigm that directly contrasted the effects of stimulus and decision changes to identify the underlying brain systems. Direct repetition of stimulus features caused marked reductions in posterior regions of the inferior temporal lobe that were insensitive to whether the decision was held constant or changed between study and test. By contrast, prefrontal cortex showed repetition effects that were sensitive to the exact stimulus-to-decision mapping. Analysis of resting-state functional connectivity revealed that the dissociated repetition effects are embedded within distinct brain systems. Regions that were sensitive to changes in the stimulus correlated with perceptual cortices, whereas the decision changes attenuated activity in regions correlated with middle-temporal regions and a frontoparietal control system. These results thus explain the long-known dissociation between perceptual and conceptual components of priming by revealing how a single experience can separately influence distinct, concurrently active brain systems.
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Intrinsic connections between brain networks have been linked to important functions such as processing speed and cognitive flexibility in health and in disease.
“which in turn have been linked to important functions such as processing speed37 and cognitive flexibility38 in health and in disease.”
From Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder (2012) · cites this paper as [38]
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Kim, M. J., Loucks, R. A., Palmer, A. L., Brown, A. C., Solomon, K. M., Marchante, A. N., & Whalen, P. J. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.025 · Cited by 838 · see citing works
Noonan, K. A., Jefferies, E., Visser, M., & Lambon Ralph, M. A. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00442 · Cited by 543 · see citing works
Sripada, R. K., King, A. P., Welsh, R. C., Garfinkel, S. N., Wang, X., Sripada, C. S., & Liberzon, I. (2012) · Psychosomatic Medicine · doi:10.1097/psy.0b013e318273bf33 · Cited by 412 · see citing works
Kim, M. J., Gee, D. G., Loucks, R. A., Davis, F. C., & Whalen, P. J. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq237 · Cited by 388 · see citing works
Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder
Sripada, R. K., King, A. P., Garfinkel, S. N., Wang, X., Sripada, C. S., Welsh, R. C., & Liberzon, I. (2012) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.110069 · Cited by 352 · see citing works
Emotion words shape emotion percepts.
Gendron, M., Lindquist, K. A., Barsalou, L. W., & Barrett, L. F. (2012) · Emotion · doi:10.1037/a0026007 · Cited by 334 · see citing works
Concepts and principles in the analysis of brain networks
Wig, G. S., Schlaggar, B. L., & Petersen, S. E. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05947.x · Cited by 280 · see citing works
Self-citationGotts, S. J., Chow, C. C., & Martin, A. (2012) · Cognitive Neuroscience · doi:10.1080/17588928.2012.670617 · Cited by 213 · see citing works
Somerville, L. H., Wagner, D. D., Wig, G. S., Moran, J. M., Whalen, P. J., & Kelley, W. M. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhr373 · Cited by 196 · see citing works
Self-citationThe suppression of repetition enhancement: A review of fMRI studies
Segaert, K., Weber, K., de Lange, F. P., Petersson, K. M., & Peter Hagoort, A. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.11.006 · Cited by 191 · see citing works
Language Control in Bilinguals: Monitoring and Response Selection
Branzi, F. M., Rosa, P. A. D., Canini, M., Costa, A., & Abutalebi, J. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv052 · Cited by 179 · see citing works
Whitney, C., Jefferies, E., & Kircher, T. T. J. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq148 · Cited by 146 · see citing works
Differential engagement of brain regions within a ‘core’ network during scene construction
Summerfield, J. J., Hassabis, D., & Maguire, E. A. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.01.022 · Cited by 139 · see citing works
Functional Connectivity and Brain Activation: A Synergistic Approach
Tomasi, D. G., Wang, R., Wang, G., & Volkow, N. D. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht119 · Cited by 91 · see citing works
Predictive coding, precision and synchrony
Friston, K. J. (2012) · Cognitive Neuroscience · doi:10.1080/17588928.2012.691277 · Cited by 82 · see citing works
Cognitive neuroscience perspective on memory: overview and summary
Sridhar, S., Khamaj, A., & Asthana, M. K. (2023) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2023.1217093 · Cited by 80 · see citing works
Repetition-related reductions in neural activity reveal component processes of mental simulation
Szpunar, K. K., St. Jacques, P. L., Robbins, C. A., Wig, G. S., & Schacter, D. L. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst035 · Cited by 79 · see citing works
Self-citationStevens, W. D., Kahn, I., Wig, G. S., & Schacter, D. L. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr273 · Cited by 70 · see citing works
Self-citationKim, H. (2016) · Human Brain Mapping · doi:10.1002/hbm.23492 · Cited by 61 · see citing works
Object repetition leads to local increases in the temporal coordination of neural responses
Gilbert, J. R. (2010) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2010.00030 · Cited by 58 · see citing works
Cushman, F. A., Murray, D., Gordon-McKeon, S., Wharton, S., & Greene, J. D. (2011) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr072 · Cited by 56 · see citing works
Multiple Forms of Learning Yield Temporally Distinct Electrophysiological Repetition Effects
Race, E., Badre, D., & Wagner, A. D. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp233 · Cited by 50 · see citing works
Horner, A. J., & Henson, R. N. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00163 · Cited by 48 · see citing works
Imaging Implicit Morphological Processing: Evidence from Hebrew
Bick, A. S., Frost, R., & Goelman, G. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21357 · Cited by 48 · see citing works
Reduced task-related suppression during semantic repetition priming in schizophrenia
Jeong, B., & Kubicki, M. R. (2010) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2009.09.005 · Cited by 41 · see citing works
Hales, J. B., & Brewer, J. B. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.07.025 · Cited by 40 · see citing works
Ballesteros, S., Bischof, G. N., Goh, J. O. S., & Park, D. C. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.09.019 · Cited by 39 · see citing works
Sugiura, M., Mano, Y., Sasaki, A. T., & Sadato, N. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21469 · Cited by 39 · see citing works
Friedman, A. K., & Weiss, K. R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1287-10.2010 · Cited by 36 · see citing works
Priming Picture Naming with a Semantic Task: An fMRI Investigation
Heath, S., McMahon, K. L., Nickels, L., Angwin, A. J., MacDonald, A. D., van Hees, S., Johnson, K., & Copland, D. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032809 · Cited by 32 · see citing works
Repetition priming and repetition suppression: Multiple mechanisms in need of testing
Gotts, S. J., Chow, C. C., & Martin, A. D. (2012) · Cognitive Neuroscience · doi:10.1080/17588928.2012.697054 · Cited by 30 · see citing works
Electrophysiological Signals of Familiarity and Recency in the Infant Brain
Snyder, K. A., Garza, J. P., Zolot, L., & Kresse, A. (2010) · Infancy · doi:10.1111/j.1532-7078.2009.00021.x · Cited by 26 · see citing works
Gotts, S. J. (2016) · Psychonomic Bulletin & Review · doi:10.3758/s13423-015-0855-y · Cited by 24 · see citing works
Laufer, I., Negishi, M., Lacadie, C., Papademetris, X., & Constable, R. T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022368 · Cited by 24 · see citing works
Neural enhancement and attenuation induced by repetitive recall
Hashimoto, T., Usui, N., Taira, M., & Kojima, S. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.03.008 · Cited by 23 · see citing works
Neural adaptation across viewpoint and exemplar in fusiform cortex
Harvey, D. Y., & Burgund, E. D. (2012) · Brain and Cognition · doi:10.1016/j.bandc.2012.04.009 · Cited by 20 · see citing works
Horner, A. J., & Henson, R. N. (2010) · Human Brain Mapping · doi:10.1002/hbm.21124 · Cited by 19 · see citing works
Feuerriegel, D., Keage, H. A. D., Rossion, B., & Quek, G. L. (2018) · Biological Psychology · doi:10.1016/j.biopsycho.2018.09.002 · Cited by 17 · see citing works
Gotts, S. J., Milleville, S. C., & Martin, A. D. (2014) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.10.041 · Cited by 15 · see citing works
Gong, L., Wang, J., Yang, X., Feng, L., Li, X., Gu, C., Wang, M., Hu, J., & Cheng, H. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00722 · Cited by 15 · see citing works
Lustig, C., & Lin, Z. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-411469-2.00008-x · Cited by 11 · see citing works
Behavioural and neural evidence for the impact of fluency context on conscious memory
Gomes, C. A., Mecklinger, A., & Zimmer, H. D. (2017) · Cortex · doi:10.1016/j.cortex.2017.04.008 · Cited by 10 · see citing works
Kark, S. M., Slotnick, S. D., & Kensinger, E. A. (2019) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2019.107277 · Cited by 10 · see citing works
No effect of hippocampal lesions on stimulus-response bindings
Henson, R. N., Horner, A. J., Greve, A., Cooper, E., Gregori, M., Simons, J. S., Erzinçlioğlu, S., Browne, G., & Kapur, N. (2017) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.07.024 · Cited by 9 · see citing works
Neural basis of implicit memory for socio-emotional information in schizophrenia
Schwartz, B. L., Vaidya, C. J., Shook, D. A., & Deutsch, S. I. (2012) · Psychiatry Research · doi:10.1016/j.psychres.2012.10.005 · Cited by 8 · see citing works
Repetition suppression and repetition priming are processing outcomes
Wig, G. S. (2012) · Cognitive Neuroscience · doi:10.1080/17588928.2012.689964 · Cited by 8 · see citing works
Self-citationInterview with Michael Gazzaniga
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Repetition priming and cortical arousal in healthy aging and Alzheimer's disease
Kane, A. E., Festa, E. K., Salmon, D. P., & Heindel, W. C. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.02.024 · Cited by 6 · see citing works
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Synchrony upon repetition: One or multiple neural mechanisms?
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Memory in Psychiatric Disorders: A Review
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The role of stimulus-response bindings in priming: multiple routes and multiple stages
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Near-field potentials index local neural computations more accurately than population spikingPreprint
Tovar, D. A., Westerberg, J. A., Cox, M. A., Dougherty, K., Wallace, M. T., Bastos, A. M., & Maier, A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.11.540026 · Cited by 1 · see citing works
Working memory, selective visual attention and hierarchical perception
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Memory: behavior and neural basis
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Consciousness and memory in amnesia and dementia
Maynard, C. R., & Budson, A. E. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-29258-3.00047-1
- Authors
- Wig, G. S., Buckner, R. L., & Schacter, D. L.
- Affiliations
- Harvard University (US)
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2009-05
- Volume
- 101
- Issue
- 5
- Pages
- 2632-2648
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- PMC
- PMC2681438
- OpenAlex
- W2092020136
- Cited by
- 62
- References
- 100
- Citations by year
- 2026: 1 · 2025: 1 · 2023: 2 · 2021: 1 · 2020: 1 · 2019: 1 · 2018: 1 · 2017: 4 · 2016: 3 · 2015: 3 · 2014: 3 · 2013: 3 · 2012: 15
- FWCI
- 6.15
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Mental Health (MH 060941, R01MH060941)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- repetition priming, perceptual priming, conceptual priming, inferior temporal lobe, prefrontal cortex, resting-state functional connectivity
- MeSH terms
- Adolescent, Adult, Analysis of Variance, Brain, Brain Mapping, Color Perception, Decision Making, Female, Humans, Image Processing, Computer-Assisted, Functional Laterality, Magnetic Resonance Imaging, Male, Oxygen, Photic Stimulation, Reaction Time, Rest, Young Adult
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