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Neural Basis of Repetition Priming During Mathematical Cognition: Repetition Suppression Or Repetition Enhancement?

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Neural Basis of Repetition Priming During Mathematical Cognition: Repetition Suppression Or Repetition Enhancement? Neural Basis of Repetition Priming during Mathematical Cognition: Repetition Suppression or Repetition Enhancement? Valorie N. Salimpoor1,2*, Catie Chang2*, and Vinod Menon2 Abstract ■ We investigated the neural basis of repetition priming (RP) region. Rather, RT improvements were directly correlated with during mathematical cognition. Previous studies of RP have fo- repetition enhancement in the hippocampus and the postero- cused on repetition suppression as the basis of behavioral fa- medial cortex [posterior cingulate cortex, precuneus, and retro- cilitation, primarily using word and object identification and splenial cortex; Brodmannʼs areas (BAs) 23, 7, and 30, classification tasks. More recently, researchers have suggested respectively], regions known to support memory formation associative stimulus-response learning as an alternate model and retrieval, and in the SMA (BA 6) and the dorsal midcingu- for behavioral facilitation. We examined the neural basis of RP late (“motor cingulate”) cortex (BA 24d), regions known to be during mathematical problem solving in the context of these important for motor learning. Furthermore, improvements in two models of learning. Brain imaging and behavioral data were RT were also correlated with increased functional connectivity acquired from 39 adults during novel and repeated presenta- of the hippocampus with both the SMA and the dorsal mid- tion of three-operand mathematical equations. Despite wide- cingulate cortex. Our findings provide novel support for the spread decreases in activation during repeat, compared with hypothesis that repetition enhancement and associated stimulus- novel trials, there was no direct relation between behavioral fa- response learning may facilitate behavioral performance during cilitation and the degree of repetition suppression in any brain problem solving. ■ INTRODUCTION the physical attributes of the stimulus, whereas concep- Repetition priming (RP) refers to facilitation in behav- tual priming is mainly related to semantic processing ioral performance upon subsequent exposure to a stim- and decision making independent of the physical attri- ulus (Henson, 2003; Henson, Shallice, & Dolan, 2000; butes. At the perceptual level, priming effects emerge Scarborough, Cortese, & Scarborough, 1977). RP has been in modality-specific cortical regions that are involved in widely used to investigate the neural and the behavioral extracting physical features of stimuli (Gilaie-Dotan, Nir, mechanisms that underlie rapid learning. In conjunction & Malach, 2008; Bergerbest, Ghahremani, & Gabrieli, with improvements in RT, stimulus repetition is often ac- 2004; Doniger et al., 2001; Grill-Spector et al., 1999). With companied by attenuation of neural responses (repetition greater cognitive demand, RS is also observed in “higher suppression; RS), which can be recorded either at the level order” cortical regions, including temporal lobe areas of single cells (Rainer & Miller, 2000; Desimone, 1996; Miller, specific to, for example, recognition of objects (Koutstaal Li, & Desimone, 1991) or across multiple brain regions et al., 2001), scenes (Bunzeck, Schutze, & Duzel, 2006; ranging from unimodal sensory to heteromodal associa- Blondin & Lepage, 2005), faces (Bunzeck et al., 2006; tion cortices (Maccotta & Buckner, 2004; Henson, 2003; Eger, Schweinberger, Dolan, & Henson, 2005), or words Buckner & Koutstaal, 1998; Buckner et al., 1995; Demb (Orfanidou, Marslen-Wilson, & Davis, 2006). Most pre- et al., 1995; Raichle et al., 1994). vious studies of RP have focused on perceptual and con- The precise location and extent of attenuation in ceptual priming of objects and words (Roediger, 2003). neural activity depends on the level of information pro- With visually presented objects, participants are typically cessing required by the task, and researchers frequently asked to decide whether images depict living or non- distinguish between perceptual and conceptual priming living objects (Wig, Grafton, Demos, & Kelley, 2005), nat- in this context. Perceptual priming is mainly related to ural or manufactured objects (Zago, Fenske, Aminoff, & Bar, 2005), indoor or outdoor scenes (Bunzeck et al., 1McGill University, Montreal, QC, Canada, 2Stanford University 2006; Turk-Browne, Yi, & Chun, 2006), and possible or School of Medicine, CA impossible objects (Habeck, Hilton, Zarahn, Brown, & *V. N. S. and C. C. contributed equally to the study. Stern, 2006). With visually presented words, participants © 2009 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 22:4, pp. 790–805 are typically asked to distinguish between living or non- parahippocampal gyrus (Turk-Browne et al., 2006), and living items (Lustig & Buckner, 2004; Maccotta & Buckner, the caudate nucleus (Bunzeck et al., 2006). Thus, the link 2004), and with words presented aurally, participants are between RS and behavioral facilitation has only been con- asked to decide whether words were real or pseudowords sistently demonstrated in the IFC. However, other studies (Gagnepain et al., 2008; Orfanidou et al., 2006) and have reported improvements in behavioral performance whether environmental sounds were made by an animal without any decreases in activity in the IFC (Eger, Henson, (Bergerbest et al., 2004). Tasks that involve semantic pro- Driver, & Dolan, 2004; Henson, Shallice, Gorno-Tempini, & cessing (e.g., retrieving conceptual information about Dolan, 2002), and individuals with lesions in the IFC (Brocaʼs words or objects) typically show RS effects in the PFC, aphasia) nonetheless demonstrate intact lexical-semantic primarily within the left inferior frontal cortex (IFC; Lustig priming (Hagoort, 1997). A further challenge to the tuning & Buckner, 2004; Maccotta & Buckner, 2004; Wagner, model is the finding that RS is not always accompanied by Gabrieli, & Verfaellie, 1997; Buckner et al., 1995; Demb behavioral improvements (Henson & Mouchlianitis, 2007; et al., 1995). Here, we examine the generalizability of find- Lin & Ryan, 2007; Ryan & Schnyer, 2007). ings from previous RP studies with a novel task involving An alternative, but not necessarily mutually exclusive, mathematical problem solving and a control task involving model has recently been proposed, which posits that per- number identification. formance enhancements during repeated stimulus presen- We investigate the neural basis of behavioral improve- tation may arise from rapid stimulus-response learning ments upon repeated processing of mathematical infor- (Schnyer, Dobbins, Nicholls, Schacter, & Verfaellie, 2006; mation in the context of two current models. The more Dobbins, Schnyer, Verfaellie, & Schacter, 2004; Logan, prominent of these models of RP, the “tuning” model 1990). Under this model, an association is formed be- (Wiggs & Martin, 1998; Desimone, 1996; Li, 1993), posits tween a stimulus and a particular response during initial that performance improvements result from concurrent stimulus presentation; during repeated presentation of reductions in neural responses (Desimone, 1996; Morton, the stimulus, the appropriate response is cued, bypassing 1969). Neuronal populations that are not essential for pro- more elaborate semantic processing that accompanied cessing the stimuli drop out of the initial cell assembly, initial stimulus presentation (Horner & Henson, 2008). In yielding more efficient processing (Wiggs & Martin, 1998; support of this model, Dobbins et al. (2004) found that de- Gupta & Cohen, 1990). Evidence for fine tuning of neuro- spite using the same stimuli upon repeated presentation, nal representations comes from the finding that brain areas changing the task rules diminished behavioral facilitation. that demonstrate RS are typically a subset of those that This study demonstrated that it was not the repeated pro- were originally involved in performing the task (Henson, cessing of the stimuli that was resulting in behavioral facili- 2003) and that RS increases with repeated stimulus pre- tation but rather the formation of an association between sentations (Sayres & Grill-Spector, 2006; Grill-Spector & the stimulus and its correct response. Behavioral facili- Malach, 2001; Henson et al., 2000). tation may therefore be more directly related to brain sys- Despite considerable evidence that repeated task per- tems that support associative learning rather than RS. It formance results in both behavioral facilitation and RS, would then be expected that associative learning would evidence supporting a link between the two has been gen- involve repetition enhancement as stimulus-response map- erally weak (McMahon & Olson, 2007). In the first place, pings are formed. Although increases in neural activity have only a relatively small number of brain imaging studies of been reported in conjunction with RP (Bunzeck et al., RP have reported examining the relation between behav- 2006; Orfanidou et al., 2006; Fiebach, Gruber, & Supp, ioral changes and RS. Of these, the most consistent findings 2005; Zago et al., 2005; Henson et al., 2000), surprisingly to date have been an association between behavioral facil- few studies have found a direct relation between behavioral itation and RS in the IFC (Gagnepain et al., 2008; Bunzeck facilitation and increased neural activity. A notable excep- et al., 2006; Orfanidou et al., 2006; Wig et al., 2005; Zago tion is the recent study by Horner and Henson (2008), et al., 2005; Bergerbest et al., 2004; Lustig & Buckner, which found that repetition enhancement within the pos- 2004; Maccotta & Buckner,
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