Reductions in cortical activity during priming
Abstract
Priming is a nonconscious form of memory in which an encounter with a stimulus influences the subsequent identification, production or classification of the same or a related stimulus. Neuroimaging studies have revealed that behavioral priming is typically accompanied by reduced activity in several cortical regions. We review recent studies that have concerned two key issues. First, specificity effects produced by changes between study and test in either the physical features of stimuli or the behavioral response reveal cortical sensitivity to the perceptual, conceptual and stimulus-to-decision mapping properties of primed items. Second, correlations between behavioral priming and activity reductions are robust across a range of tasks and procedures in prefrontal regions but not in posterior regions. On the basis of these recent studies, we suggest that the reduction in cortical activity during priming involves at least two different mechanisms.
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Prior literature indicates that neural activity usually decreases when stimuli and tasks are repeated, a repetition suppression effect.
“This finding is particularly noteworthy given the extensive literature showing that neural activity typically decreases when stimuli and tasks are repeated (i.e., repetition suppression; Grill-Spector et al., 2006; Schacter et al., 2007).”
From Neural systems supporting lexical search guided by letter and semantic category cues: a self-paced overt response fMRI study of verbal fluency (2010) · cites this paper as Schacter et al., 2007
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BackgroundResultNeural Response Suppression Predicts Repetition Priming of Spoken Words and Pseudowords
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“We identified more activity in the right anterior hippocampus, fusiform gyrus, right visual cortex and left prefrontal cortex (PFC) in response to novel scenes, an effect often seen in neural priming studies comparing brain responses to novel and repeated stimuli (Schacter et al., 2007).”
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BackgroundMultiple signals of recognition memory in the medial temporal lobe
Yassa, M. A., & Stark, C. E. L. (2008) · Hippocampus · doi:10.1002/hipo.20452 · Cited by 78 · see citing works
“…1995; Desimone, 1996; Buckner et al., 1998a,b; Wiggs and Martin, 1998; Maccotta and Buckner, 2004; Law et al., 2005; Grill-Spector et al., 2006; Schacter et al., 2007) as well as increases (Konishi et al., 2000; McDermott et al., 2000; Gonsalves et al., 2005; Law et al., 2005; Wagner et al.…”
BackgroundMethodScene Representations in Parahippocampal Cortex Depend on Temporal Context
Turk‐Browne, N. B., Simon, M. G., & Sederberg, P. B. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0942-12.2012 · Cited by 75 · see citing works
“Moreover, behavioral priming is often more correlated with RA in prefrontal cortex than in visual cortex (Schacter et al., 2007).”
BackgroundDissociating Task Performance from fMRI Repetition Attenuation in Ventral Visual Cortex
Yaoda Xu, A., Turk‐Browne, N. B., & Chun, M. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5527-06.2007 · Cited by 72 · see citing works
“These results also indicate that the neural mechanisms underlying fMRI repetition attenuation may be different across brain regions, consistent with Schacter et al. (2007).”
ResultKróliczak, G., McAdam, T. D., Quinlan, D. J., & Culham, J. C. (2008) · Journal of Neurophysiology · doi:10.1152/jn.01376.2007 · Cited by 72 · see citing works
The neural correlates of conceptual and perceptual false recognitionPreprint
Garoff-Eaton, R. J., Kensinger, E. A., & Schacter, D. L. (2007) · Learning & Memory · doi:10.1101/lm.695707 · Cited by 72 · see citing works
Schendan, H. E., & Ganis, G. (2012) · Frontiers in Psychology · doi:10.3389/fpsyg.2012.00329 · Cited by 69 · see citing works
“, 2006), and top-down processes from the frontal lobe, which support mental imagery, have been implicated in perceptual repetition priming (Schacter et al., 2007).”
BackgroundVoss, J. L., Federmeier, K. D., & Paller, K. A. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr315 · Cited by 71 · see citing works
Stevens, W. D., Kahn, I., Wig, G. S., & Schacter, D. L. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr273 · Cited by 70 · see citing works
A single-system account of the relationship between priming, recognition, and fluency.
Berry, C. J., Shanks, D. R., & Henson, R. N. (2008) · Journal of Experimental Psychology Learning Memory and Cognition · doi:10.1037/0278-7393.34.1.97 · Cited by 67 · see citing works
Pourtois, G., Schwartz, S., Spiridon, M., Martuzzi, R., & Vuilleumier, P. O. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn210 · Cited by 66 · see citing works
“At the brain level, a reduction in neuronal activity is observed for repeated exposures relative to initial presentations, a phenomenon known as neural priming (Schacter et al. 2007), adaptation (Grill-Spector and Malach 2001), or repetition suppression (Desimone 1996).”
BackgroundInfluentialLearning and Recognition of a Non-conscious Sequence of Events in Human Primary Visual Cortex
Rosenthal, C. R., Andrews, S. K., Antoniades, C. A., Kennard, C., & Soto, D. (2016) · Current Biology · doi:10.1016/j.cub.2016.01.040 · Cited by 64 · see citing works
“Furthermore, the non-conscious recognition effect seen here is distinguished from other non-conscious forms of memory, such as repetition priming, because repetition-related occipital fluency effects (1) are often unrelated to behavior [40], (2) if present, only prime a particular response such as identification [41],…”
BackgroundWig, G. S., Buckner, R. L., & Schacter, D. L. (2009) · Journal of Neurophysiology · doi:10.1152/jn.91213.2008 · Cited by 62 · see citing works
“Consistent with previous demonstrations of response learning (Dobbins et al. 2004; Schnyer et al. 2007), behavioral priming was significantly greater during classification of old objects while participants performed the same-decision relative to classification of old items when the response was…”
ResultSelf-citationEstablishing a relationship between activity reduction in human perirhinal cortex and priming
Voss, J. L., Hauner, K. K. Y., & Paller, K. A. (2009) · Hippocampus · doi:10.1002/hipo.20608 · Cited by 63 · see citing works
“visual cortex, and facilitated strategic processing in left prefrontal cortex (Schacter et al., 2007).”
BackgroundKim, H. (2016) · Human Brain Mapping · doi:10.1002/hbm.23492 · Cited by 61 · see citing works
“…multiple network configuration supports the hypothesis that the repetition suppression effects observed across the diverse cortical regions reflect multiple distinct mechanisms operating somewhat independently rather than as a single unitary process [Henson, 2016; r 1903 r Schacter et al., 2007].”
BackgroundResultInfluentialObject 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
Zhang, J. X., Fang, Z., Du, Y., Kong, L., Zhang, Q., & Xing, Q. (2012) · Chinese Science Bulletin · doi:10.1007/s11434-011-4932-y · Cited by 56 · see citing works
A role for the perceptual representation memory system in category learning
CASALE, M. B., & Ashby, F. G. (2008) · Perception & Psychophysics · doi:10.3758/pp.70.6.983 · Cited by 57 · see citing works
“On the other hand, such deactivations are typically not correlated with behavioral measures ( Schacter, Wig, & Stevens, 2007 ), so the neuroimaging data do not speak to the question of whether the PRS is mediating prototype distortion learning.”
BackgroundNeural signatures of test-potentiated learning in parietal cortex
Nelson, S. M., Arnold, K. M., Gilmore, A. W., & McDermott, K. B. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0960-13.2013 · Cited by 57 · see citing works
“This pattern would be similar to findings in the implicit memory literature, in which repeated processing of items is accompanied by “repetition suppression,” sometimes also referred to as “neural priming” (Buckner et al., 2000; Schacter et al., 2007).”
ResultThe time course of repetition effects for familiar faces and objects: An ERP study
Guillaume, C., Guillery‐Girard, B., Chaby, L., Lebreton, K., Hugueville, L., Eustache, F., & Fiori, N. (2008) · Brain Research · doi:10.1016/j.brainres.2008.10.069 · Cited by 56 · see citing works
“Moreover, some authors have demonstrated that only certain neural repetition effects are specifically correlated with behavioural priming (see Schacter et al., 2007 for review).”
BackgroundCognitive function in normal aging and in older adults with mild cognitive impairment
Ballesteros, S., Mayas, J., & Reales, J. (2013) · Psicothema · doi:10.7334/psicothema2012.181 · Cited by 56 · see citing works
“Functional magnetic resonance (fMRI) studies of repetition priming when a fully attended stimulus was presented at encoding found reduced brain activation for repeated visual stimuli compared to new stimuli in brain areas that code for repeated stimulus properties (Schacter et al., 2007; Henson, 2003).”
BackgroundBallesteros, S., Avilés, J. M. R., Mayas, J., & Heller, M. A. (2008) · Experimental Brain Research · doi:10.1007/s00221-008-1441-6 · Cited by 53 · see citing works
“This reduction in activation has been referred to as ‘‘repetition suppression’’ (RS) and has been associated with repetition priming (see Henson 2003; Schacter et al. 2007; Vuilleumier et al. 2005).”
BackgroundFunctional Magnetic Resonance Adaptation in Visual Neuroscience
Weigelt, S., Muckli, L. F., & Kohler, A. (2008) · Reviews in the Neurosciences · doi:10.1515/revneuro.2008.19.4-5.363 · Cited by 53 · see citing works
Escaping the Past: Contributions of the Hippocampus to Future Thinking and Imagination
Schacter, D. L., Addis, D. R., & Szpunar, K. K. (2017) · The Hippocampus from Cells to Systems · doi:10.1007/978-3-319-50406-3_14 · Cited by 54 · see citing works
“…phase) in a core network of regions that was similarly active when participants remembered the past and imagined the future, including medial prefrontal, medial temporal, and posterior parietal cortices (for discussion of this core network, see Benoit and Schacter 2015; Schacter et al. 2007a).”
BackgroundInfluentialSelf-citationMultiple 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
Emberson, L. L., Cannon, G., Palmeri, H., Richards, J. E., & Aslin, R. Ν. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2016.11.002 · Cited by 51 · see citing works
“The other mechanism “primarily reflects hanges in the prefrontal cortex [and these changes] drive behavoral priming effects in a top-down manner” (Schacter et al., 2007, .”
InfluentialHow the Neuroscience of Decision Making Informs Our Conception of Autonomy
Felsen, G., & Reiner, P. B. (2011) · AJOB Neuroscience · doi:10.1080/21507740.2011.580489 · Cited by 50 · see citing works
“To address this question, we briefly apply the principles discussed earlier to decisions made in four contexts in which autonomy has been a topic of debate.”
MethodKupers, R. C., & Ptito, M. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53355-5.00002-6 · Cited by 51 · see citing works
Recollective performance advantages for implicit memory tasks
Sheldon, S., & Moscovitch, M. (2010) · Memory · doi:10.1080/09658211.2010.499876 · Cited by 49 · see citing works
“To reconcile these discrepant findings, Schacter, Wig, and Stevens ( 2007 ; see also Shacter, et al, 2004) proposed two different types of priming: one that relies on cortical-perceptual representations, independent of the MTL or explicit memory, and another that relies on MTL-based operations which are involved in es…”
Cognitive Neuroscience of Memory
Slotnick, S. D. (2017) · Cambridge University Press eBooks · doi:10.1017/9781316026687 · Cited by 48 · see citing works
Jiang, J., Brashier, N. M., & Egner, T. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2957-15.2015 · Cited by 44 · see citing works
“Moreover, selective stimulus category binding effects were observed in posterior frontal cortex, notably including inferior frontal gyrus, which has in the past been implicated in the priming of concepts and abstract features (Schacter et al., 2007).”
BackgroundA critical role of the human hippocampus in an electrophysiological measure of implicit memory
Addante, R. J. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2014.12.069 · Cited by 46 · see citing works
“In support of this view is that the negative ERP effect in patients resembles repetition suppression effects seen in other modalities (Buckner et al., 1995; Dobbins et al., 2004; Gotts et al., 2012a,b; Schacter et al., 2007; Wig et al., 2005; Henson, 2003).”
BackgroundResultInfluentialGagnepain, P., Henson, R. N., Chételat, G., Desgranges, B., Lebreton, K., & Eustache, F. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21454 · Cited by 44 · see citing works
“Priming normally elicits reduced activity in the cortical regions associated with processing those stimuli, a reduction that is often attributed to more efficient processing (eg, Schacter, Wig, & Stevens, 2007 ; Henson, 2003 ).”
BackgroundSoto, D., Llewelyn, D., & Silvanto, J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6243-11.2012 · Cited by 44 · see citing works
“Repetition attenuation in visual cortex is very specific to the properties of the visual representation and has not been associated with high-level priming and behavioral response facilitation (Schacter et al., 2007).”
BackgroundLucas, H. D., Taylor, J. R., Henson, R. N., & Paller, K. A. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.07.036 · Cited by 42 · see citing works
“Indeed, priming is known to have multiple subtypes driven by dissociable forms of fluency, the most well-studied of which are conceptual and perceptual fluency (Henson, 2003; Schacter, Wig, & Stevens, 2007).”
Ageing, cognition, and neuroscience: An introduction
Ballesteros, S., Nilsson, L., & Lemaire, P. (2009) · The European Journal of Cognitive Psychology · doi:10.1080/09541440802598339 · Cited by 44 · see citing works
“Research on implicit memory has interested cognitive psychologists and neuroscientists for many years because empirical findings have shown consistently that this type of memory assessed by repetition priming is dissociable of explicit memory measures such a recognition or recall (eg, Cooper, Schacter, Ballesteros, &…”
BackgroundKim, H. (2019) · Biological Psychology · doi:10.1016/j.biopsycho.2019.04.006 · Cited by 40 · 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
“This region has been shown tobeessentialfortherepetitionprimingeffect(Thieletal., 2005; Wig, Grafton, Demos, & Kelley, 2005) and seems to play a role in linking retrieved person-selective information with behavioral responses(Wig, Buckner,& Schacter, 2009; Schacter, Wig, & Stevens, 2007 ).”
BackgroundBallesteros, 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
“processes, as a reflection of more efficient neural processing when encountering the same visual information again (Grill-Spector et al., 2006; Henson, 2003; Martin, 2007; Schacter et al., 2007; Wig et al., 2009).”
BackgroundReal-Time Neural Signals of Perceptual Priming with Unfamiliar Geometric Shapes
Voss, J. L., & Paller, K. A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0403-10.2010 · Cited by 38 · see citing works
“Priming in the visual modality has been associated with changes in neural processing in extrastriate visual cortex (Wiggs and Martin, 1998; Henson, 2003; Schacter et al., 2007).”
BackgroundMethodInfluentialFriese, U., Supp, G. G., Hipp, J. F., Engel, A. K., & Gruber, T. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.07.073 · Cited by 38 · see citing works
“Schacter et al. (2007) proposed that, for visual stimuli, perceptual cortices show a gradient of stimulus specificity with greater specificity occurring in posterior regions compared to more anterior sites.”
InfluentialGold, C. A., Marchant, N. L., Koutstaal, W., Schacter, D. L., & Budson, A. E. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2007.04.021 · Cited by 37 · see citing works
Action-Based Learning of Multistate Objects in the Medial Temporal Lobe
Hindy, N. C., & Turk‐Browne, N. B. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv030 · Cited by 34 · see citing works
“These studies consistently report attenuated activity in LO for repeated versus novel stimuli (Schacter et al. 2007), with growing evidence for increased repetition attenuation when repeated stimuli are expected versus unexpected (Summerfield et al. 2008; Larsson and Smith 2012); these latter…”
BackgroundDistinct Neural Suppression and Encoding Effects for Conceptual Novelty and Familiarity
Reggev, N., Bein, O., & Maril, A. (2016) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00994 · Cited by 35 · see citing works
“(Schacter, Wig, & Stevens, 2007), novel pairs should be associated with increased RS.”
BackgroundAlzheimer's disease and implicit memory
Machado, S. E. D. C., da Cunha, M. M., Minc, D., Portella, C. E., Velasques, B., Basile, L., Cagy, M., Piedade, R. A. M., & Ribeiro, P. F. M. (2009) · Arquivos de Neuro-Psiquiatria · doi:10.1590/s0004-282x2009000200034 · Cited by 35 · see citing works
Word Semantics Is Processed Even without Attentional Effort
Relander, K., Pia Rämä, A., & Kujala, T. (2008) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21127 · Cited by 35 · see citing works
“Similarly, in fMRI studies, behavioral priming is associated with reduced activity in several cortical regions (e.g., Schacter, Wig, & Stevens, 2007; Henson, 2003).”
BackgroundMemory before and after H.M.: an impressionistic historical perspective
Moscovitch, M. (2012) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199580286.003.0002 · Cited by 34 · see citing works
Remembering that big things sound big: Sound symbolism and associative memory
Preziosi, M. A., & Coane, J. H. (2017) · Cognitive Research Principles and Implications · doi:10.1186/s41235-016-0047-y · Cited by 37 · see citing works
Implicit Memory, Constructive Memory, and Imagining the Future: A Career Perspective
Schacter, D. L. (2018) · Perspectives on Psychological Science · doi:10.1177/1745691618803640 · Cited by 33 · see citing works
Enhancement and suppression in a lexical interference fMRI‐paradigm
Abel, S., Dressel, K., Weiller, C., & Huber, W. (2012) · Brain and Behavior · doi:10.1002/brb3.31 · Cited by 31 · see citing works
“Moreover, the behavioral effect in conceptual priming has shown to be associated with repetition suppression in left IFG (Wig et al. 2005; Orfanidou et al. 2006; Schacter et al. 2007); an according association with right IFG has also been reported (Bergerbest et al.”
BackgroundInfluentialAge differences in the neural correlates of novelty processing: The effects of item-relatedness
Bowman, C. R., & Dennis, N. A. (2014) · Brain Research · doi:10.1016/j.brainres.2014.08.006 · Cited by 33 · see citing works
“…that young, but not older adults recruited regions of early visual cortex for related novelty success given this region's importance to low-level visual processing that has been shown to support true memories, and speci fi cally true recollections (Dennis et al., 2012; Slotnick and Schacter, 2004).”
BackgroundMethodInfluentialLamy, D., Mudrik, L., & Deouell, L. Y. (2007) · Consciousness and Cognition · doi:10.1016/j.concog.2007.11.001 · Cited by 31 · see citing works
Priming tool actions: Are real objects more effective primes than pictures?
Squires, S. D., Macdonald, S. N., Culham, J. C., & Snow, J. C. (2015) · Experimental Brain Research · doi:10.1007/s00221-015-4518-z · Cited by 31 · see citing works
Salimpoor, V. N., Chang, C. E., & Menon, V. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21234 · Cited by 29 · see citing works
“No brain regions showed significantly greater activation during the repeat compared with the novel stimulus presentation.”
BackgroundNeural mechanisms of repetition priming of familiar and globally unfamiliar visual objects
Soldan, A., Habeck, C. G., Gazes, Y., & Stern, Y. (2010) · Brain Research · doi:10.1016/j.brainres.2010.04.071 · Cited by 28 · see citing works
FMRI adaptation during performance of learned arbitrary visuomotor conditional associations
Chouinard, P. A., & Goodale, M. A. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.07.020 · Cited by 28 · see citing works
“…(e.g. Dinstein et al., 2007; Chouinard et al., 2009) as well as in highlevel cognitive operations such as those involved in memory and language (for review, see Schacter et al., 2007), action recognition (Chong et al., 2008; Lingnau et al., 2009), and illusory percepts (Chouinard et al., 2009).”
- Authors
- Schacter, D. L., Wig, G. S., & Stevens, W. D.
- Affiliations
- Harvard University (US)
- Corresponding author
- Schacter, Daniel L
- Venue
- Current Opinion in Neurobiology
- Publisher
- Elsevier BV
- Published
- 2007-04
- Volume
- 17
- Issue
- 2
- Pages
- 171-176
- ISSN
- 0959-4388 (ISSN-L)
- OpenAlex
- W2015144099
- Cited by
- 270
- References
- 48
- Citations by year
- 2025: 2 · 2024: 1 · 2023: 5 · 2022: 2 · 2021: 9 · 2020: 7 · 2019: 8 · 2018: 7 · 2017: 25 · 2016: 13 · 2015: 20 · 2014: 15 · 2013: 20 · 2012: 31
- FWCI
- 2.15
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Current Opinion in Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (AG 08441)
- 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 › Neurobiology of Language and Bilingualism
- Keywords
- behavioral priming, prefrontal cortex, stimulus specificity
- MeSH terms
- Brain Mapping, Cerebral Cortex, Decision Making, Humans, Memory, Perception, Physical Stimulation, Unconscious, Psychology
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