Repetition-related reductions in neural activity reveal component processes of mental simulation

doi:10.1093/scan/nst035 SCAN (2014) 9, 712^722 Repetition-related reductions in neural activity reveal component processes of mental simulation Karl K. Szpunar,1,2 Peggy L. St. Jacques,1,2 Clifford A. Robbins,1 Gagan S. Wig,3 and Daniel L. Schacter1,2 1 Department of Psychology, Harvard University, 33 Kirkland Street, Cambridge, MA 02138, USA, 2Center for Brain Science, Harvard University, 33 Kirkland Street, Cambridge, MA 02138, USA, and 3Department of Neurology, Washington University School of Medicine, 4525 Scott Avenue, St. Louis, MO 63110, USA In everyday life, people adaptively prepare for the future by simulating dynamic events about impending interactions with people, objects and locations. Previous research has consistently demonstrated that a distributed network of frontal–parietal–temporal brain regions supports this ubiquitous mental activity. Nonetheless, little is known about the manner in which specific regions of this network contribute to component features of future simulation. In two experiments, we used a functional magnetic resonance (fMR)-repetition suppression paradigm to demonstrate that distinct frontal–parietal–temporal regions are sensitive to processing the scenarios or what participants imagined was happening in an event (e.g. medial prefrontal, posterior cingulate, temporal–parietal and middle temporal cortices are sensitive to the scenarios associated with future social events), people (medial prefrontal cortex), objects (inferior frontal and premotor cortices) and locations (posterior cingulate/retrosplenial, parahippocampal and posterior parietal cortices) that typically constitute simulations of personal future events. This pattern of results demonstrates that the neural substrates of these component features of event simulations can be reliably identified in the context of a task that requires participants to simulate complex, everyday future experiences. Keywords: future event simulation; fMRI; repetition suppression; default network INTRODUCTION A growing number of neuroimaging studies have delineated neural correlates of the capacity to imagine or simulate future events. These studies of future event simulation have revealed that a distributed network of frontal–parietal–temporal brain regions underlies the flexible capacity to simulate hypothetical events that may one day come to pass in the personal future (Schacter et al., 2008; Szpunar, 2010). In a recent review of the literature, Schacter et al. (2012) noted that an important limitation of existing studies has been the use of relatively unconstrained task designs that do not readily allow the identification of component processes of future event simulation. For instance, simulated future events typically consist of scenarios that involve interactions with familiar people, objects and locations (D’Argembeau and Van der Linden, 2012), yet there has been little progress in identifying and distinguishing among these key components of future event simulations. A more complete and detailed understanding of future event simulation will require the development of paradigms that can systematically isolate the contributions of specific brain regions to specific features of future simulation (for initial attempts, see Hassabis et al., 2007; Szpunar et al., 2009; Andrews-Hanna et al., 2010a). Here, we present a paradigm in which the content and frequency of simulated future events were systematically varied in order to evoke content-specific repetition-related reductions in neural activity. Functional magnetic resonance (fMR)-repetition suppression is a technique that evokes repetition-related reductions in neural activity to demonstrate that specific regions of the brain are sensitive to processing specific classes of stimuli (Grill-Spector et al., 2006; Schacter et al., 2007b). For instance, fMR-repetition suppression has been used to demonstrate that distinct regions of the medial temporal lobe are sensitive to the initial, relative to repeated, processing of objects and Received 13 December 2012; Accepted 21 February 2013 Advance Access publication 11 March 2013 This research was supported by National Institute of Mental Health Grant 5R01MH60941-13, awarded to Daniel L. Schacter. Correspondence should be addressed to Karl K. Szpunar, Department of Psychology, Harvard University, 33 Kirkland Street, Cambridge, MA 02138. E-mail: scenes (Litman et al., 2009), or items and their context (Diana et al., 2012). Although much of this research has been conducted within the domain of perceptual processing, the technique has been extended to identify processes involved in making self-other judgments (Jenkins et al., 2008), and more recently to distinguish between novel and repeated future event simulations (V. van Mulukom et al., submitted for publication). We propose that manipulating the content of future event simulation (e.g. whether a future event involves interacting with another person or object) and the frequency with which specific features of that content are simulated (e.g. people, objects and locations) can elucidate which brain regions support which aspects of future event simulation in the context of a complex simulation task. Across two experiments, participants simulated future social (Exp. 1) or non-social (Exp. 2) events, and we manipulated the frequency with which familiar people (Exp. 1), objects, (Exp. 2) and locations (Exps 1 and 2) were included in those simulations. An advantage of directly manipulating the presentation of people, objects and locations in the context of future simulation is that the extensive research on these component features in non-simulation contexts allowed us to make informed predictions about how various frontal–parietal–temporal brain regions would contribute to the construction of complex event simulations. In particular, we made three predictions. First, simulated social (Exp. 1), but not non-social (Exp. 2), scenarios (i.e. what the participant imagines happening in an event) should preferentially engage a distributed set of medial prefrontal, parietal and lateral temporal regions commonly activated during tasks that focus attention on socially relevant interactions (Hari and Kujala, 2009; Van Overwalle, 2009). Second, simulations involving people (Exp. 1) and objects (Exp. 2) should preferentially engage regions commonly activated by tasks that focus attention on conceptual features of people and objects (such as middle and inferior frontal gyrus, respectively; Wig et al., 2009; Raposo et al., 2011). Third, simulated locations (Exps 1 and 2) should preferentially engage regions commonly activated by tasks that focus attention on scenes (i.e. parahippocampal and retrosplenial cortices; Epstein, 2008). However, activity in parahippocampal cortex should be more pronounced during non-social events as simulations of object use (Exp. 2), more so than interpersonal interactions ß The Author (2013). Published by Oxford University Press. For (...truncated)