Cognitive Neuroscience ISSN: 1758-8928 (Print) 1758-8936 (Online) Journal homepage: https://www.tandfonline.com/loi/pcns20 Repetition suppression and repetition priming are processing outcomes Gagan S. Wig To cite this article: Gagan S. Wig (2012) Repetition suppression and repetition priming are processing outcomes, Cognitive Neuroscience, 3:3-4, 247-248, DOI: 10.1080/17588928.2012.689964 To link to this article: https://doi.org/10.1080/17588928.2012.689964 Published online: 27 Jul 2012. Submit your article to this journal Article views: 119 Citing articles: 4 View citing articles Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=pcns20 COGNITIVE NEUROSCIENCE, 2012, 3 (3–4), 227–259 (includes Discussion Paper, Commentaries, and Reply) Discussion Paper Repetition priming and repetition suppression: A case for enhanced efficiency through neural synchronization Stephen J. Gotts1, Carson C. Chow2, and Alex Martin1 1Section on Cognitive Neuropsychology, Laboratory of Brain and Cognition, National Institute of Mental Health (NIMH), National Institutes of Health, Bethesda, MD, USA 2Laboratory of Biological Modeling, National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), National Institutes of Health, Bethesda, MD, USA Stimulus repetition in identification tasks leads to improved behavioral performance (“repetition priming”) but attenuated neural responses (“repetition suppression”) throughout task-engaged cortical regions. While it is clear that this pervasive brain–behavior relationship reflects some form of improved processing efficiency, the exact form that it takes remains elusive. In this Discussion Paper, we review four different theoretical proposals that have the potential to link repetition suppression and priming, with a particular focus on a proposal that stimulus repetition affects improved efficiency through enhanced neural synchronization. We argue that despite exciting recent work on the role of neural synchronization in cognitive processes such as attention and perception, similar studies in the domain of learning and memory ––and priming, in particular––have been lacking. We emphasize the need for new studies with adequate spatiotemporal resolution, formulate several novel predictions, and discuss our ongoing efforts to disentangle the current proposals. Keywords: Repetition priming; Repetition suppression; Synchrony; Prediction; Expectation. When we repeatedly encounter an object in the envir- it often occurs without subjects’ awareness (e.g., Cave onment, we become faster and more accurate at identi- & Squire, 1992) and is robust to attentional manipula- fying it, a phenomenon referred to as “repetition tions (e.g., Kellogg, Newcombe, Kammer, & Schmitt, priming” (see Schacter & Buckner, 1998; Tulving & 1996; Szymanski & MacLeod, 1996) and modest Schacter, 1990, for review). Repetition priming is alterations of stimulus form (e.g., Biederman & stimulus-specific, builds up over several stimulus repe- Cooper, 1991, 1992; Cave, Bost, & Cobb, 1996; titions (e.g., Logan, 1990; Ostergaard, 1998; Wiggs, Srinivas, 1996). Historically, repetition priming has Martin, & Sunderland, 1997), and while it attenuates played an important role in our understanding of the over short delays (e.g., McKone, 1995, 1998), it can be organization of human memory due to its neuropsy- extremely long-lasting with significant residual effects chological dissociation from more explicit forms of lasting days, months, and even years (e.g., Cave, 1997; memory in amnesic patients (e.g., Graf, Squire, & Mitchell, 2006; van Turennout, Ellmore, & Martin, Mandler, 1984; Warrington & Weiskrantz, 1974). 2000). It is also relatively automatic in the sense that Amnesic patients with damage to the medial temporal Correspondence should be addressed to: Stephen J. Gotts, Section on Cognitive Neuropsychology, Laboratory of Brain and Cognition, National Institute of Mental Health (NIMH), National Institutes of Health, Bethesda, MD 20892, USA. E-mail: [email protected] The authors would like to thank Nathan Crone, David Plaut, Jay McClelland, David McMahon, Carl Olson, and Avniel Ghuman for helpful discussions. The preparation of this paper was supported by the National Institute of Mental Health, NIH, Division of Intramural Research. This work was authored as part of the Contributors’ official duties as Employees of the United States Government and is therefore a work of the United States Government. In accordance with 17 U.S.C. 105, no copyright protection is available for such works under U.S. Law. www.psypress.com/cognitiveneuroscience http://dx.doi.org/10.1080/17588928.2012.670617 228 GOTTS, CHOW, MARTIN lobes, including the hippocampus, can exhibit pro- (e.g., Schacter & Buckner, 1998; Wiggs & Martin, found impairments in recall and recognition of recent 1998). Given the automatic nature and generality of the events while at the same time demonstrating normal or two phenomena throughout different cognitive domains, nearly normal repetition priming effects (see Squire, tasks, and brain regions, the promise of understanding 1992, for review). While caution is warranted in attri- this link is that it could pay large dividends in under- buting priming entirely to implicit as opposed to expli- standing the basic relationships between brain and mind. cit memory processes (both would typically However, the relationship between repetition prim- be expected to contribute in normal individuals–– ing and repetition suppression also presents a major e.g., Henson & Gagnepain, 2010; Voss & Paller, puzzle: How is it that reductions in neural activity can 2008), the basic dissociation has led researchers to mediate better behavioral performance? After all, the focus primarily on the role of neocortical plasticity propagation of neural activity from sensory areas mechanisms, with priming potentially serving as a through to decision- and response-related brain regions window into the formation of long-term knowledge (ultimately in motor cortex) is what is thought to med- representations that reside primarily in the neocortex iate performance in an identification task. In studies of (e.g., McClelland, McNaughton, & O’Reilly, 1995; repetition priming using common objects and other Stark & McClelland, 2000). Indeed, stimulus repetition familiar stimuli, there is little evidence of repetition- paradigms in neuroimaging studies (e.g., functional related increases in neural activity (see Henson, 2003, magnetic resonance imaging, or fMRI) are routinely for review). So where does the behavioral facilitation used as a tool to infer the nature of neocortical repre- come from? Just to highlight how puzzling this basic sentations in a variety of cognitive domains situation is, it is worth remembering that the major (e.g., Andresen, Vinberg, & Grill-Spector, 2009; “activation-based” theories of priming that existed Bedny, McGill, & Thompson-Schill, 2008; Cant, prior to the first neuroimaging studies of priming in Large, McCall, & Goodale, 2008; Fairhall, Anzellotti, the mid-1990s (e.g., spreading activation, connection- Pajtas, & Caramazza, 2011; Gold, Balota, Kirchhoff, & ist models) posited repetition-related accumulation or Buckner, 2005; Gotts, Milleville, Bellgowan, & increases in activity in the nodes or units that repre- Martin, 2011; Konen & Kastner, 2008; Mahon et al., sented a given stimulus (e.g., Anderson, 1983; Becker, 2007; Piazza, Izard, Pinel, Le Bihan, & Dehaene, Moscovitch, Behrmann, & Joordens, 1997; Collins & 2004). Recent work has identified separate contribu- Loftus, 1975; McClelland & Rumelhart, 1985). This tions of perceptual, conceptual, and decision/response- issue would also appear to cut across the distinction related processing to both task performance and prim- between implicit versus explicit memory, since both ing effects (e.g., Dobbins, Schnyer, Verfaellie, & sets of processes are likely to be reflected in some Schacter, 2004; Horner & Henson, 2008, 2012; Wig, mixture in neural and behavioral repetition effects. Buckner, & Schacter, 2009; Race, Badre, & Wagner, One must still explain how less neural activity some- 2010; Race, Shanker, & Wagner, 2009 Wig, Grafton, how produces a more effective behavioral response. It Demos, & Kelley, 2005). is worth noting that in a variety of cognitive domains While behavioral performance improves with stimu- that do not intrinsically involve stimulus repetition lus repetition, neural activity in humans (BOLD fMRI) (e.g., attention, visual search, working memory, motion and monkeys (single-cell firing rates) tends to decrease, a discrimination) better behavioral performance is phenomenon often referred to as “repetition suppres- generally associated with increased rather than sion” (see Desimone, 1996; Henson, 2003; Grill- decreased activity in cells that prefer a stimulus, loca- Spector, Henson, & Martin, 2006, for reviews). Like tion, or response (e.g., Luck, Chelazzi, Hillyard, & priming, repetition suppression is stimulus-specific, Desimone, 1997; Newsome, Britten, & Movshon, builds up over several repetitions (e.g., Jiang, Haxby, 1989; Rainer, Asaad, & Miller, 1998; Schall & Hanes, Martin, Ungerleider, & Parasuraman, 2000; Miller, 1993). Indeed, the basic logic used in mapping visual Gochin, & Gross, 1991), and has both short-lived and receptive fields in single-unit studies, in evaluating the long-lasting components (e.g., Grill-Spector & Malach, results of functional localizers in neuroimaging studies, 2001; Li,