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Role of the Hippocampus and Orbitofrontal Cortex During the Disambiguation of Social Cues in Working Memory

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Role of the Hippocampus and Orbitofrontal Cortex During the Disambiguation of Social Cues in Working Memory Cogn Affect Behav Neurosci DOI 10.3758/s13415-013-0170-x Role of the hippocampus and orbitofrontal cortex during the disambiguation of social cues in working memory Robert S. Ross & Matthew L. LoPresti & Karin Schon & Chantal E. Stern # Psychonomic Society, Inc. 2013 Abstract Human social interactions are complex behaviors two faces from the same individual with different facial ex- requiring the concerted effort of multiple neural systems to pressions were presented at sample. In the nonoverlapping track and monitor the individuals around us. Cognitively, condition, the two sample faces were from two different in- adjusting our behavior on the basis of changing social cues dividuals with different expressions. fMRI activity was such as facial expressions relies on working memory and the assessed by contrasting the overlapping and nonoverlapping ability to disambiguate, or separate, the representations of conditions at sample, delay, and test. The lateral orbitofrontal overlapping stimuli resulting from viewing the same indi- cortex showed increased fMRI signal in the overlapping con- vidual with different facial expressions. We conducted an dition in all three phases of the delayed match-to-sample task fMRI experiment examining the brain regions contributing and increased functional connectivity with the hippocampus to the encoding, maintenance, and retrieval of overlapping when encoding overlapping stimuli. The hippocampus identity information during working memory using a de- showed increased fMRI signal at test. These data suggest that layed match-to-sample task. In the overlapping condition, lateral orbitofrontal cortex helps encode and maintain repre- sentations of overlapping stimuli in working memory, where- R. S. Ross : M. L. LoPresti : K. Schon : C. E. Stern as the orbitofrontal cortex and hippocampus contribute to the Center for Memory and Brain, Boston University, successful retrieval of overlapping stimuli. We suggest that the Boston, MA 02215, USA lateral orbitofrontal cortex and hippocampus play a role in encoding, maintaining, and retrieving social cues, especially R. S. Ross : M. L. LoPresti : K. Schon : C. E. Stern Center of Excellence for Learning in Education, Science, when multiple interactions with an individual need to be and Technology—CELEST, Boston University, disambiguated in a rapidly changing social context in order Boston, MA 02215, USA to make appropriate social responses. : : : R. S. Ross M. L. LoPresti K. Schon C. E. Stern . Department of Psychology, Boston University, Keywords Prefrontal Social interaction fMRI Delayed Boston, MA 02215, USA match-to-sample R. S. Ross : M. L. LoPresti : K. Schon : C. E. Stern Athinoula A. Martinos Center for Biomedical Imaging, The ability to perceive, maintain, and distinguish between Massachusetts General Hospital and Harvard Medical School, different instances of encountering an individual is critical Charlestown, MA 02129, USA from both memory and social cognition perspectives. For example, in addition to being able to recognize a friend and C. E. Stern Department of Radiology, Massachusetts General Hospital distinguish one friend from another, it is also important that and Harvard Medical School, Charlestown, MA 02129, USA we identify changing moods in individuals by separately encoding changing facial expressions over both short- and * R. S. Ross ( ) long-term social interactions. The hippocampus and Boston University, 2 Cummington Mall, Room 109, Boston, MA 02215, USA orbitofrontal cortex may be critical to guiding appropriate e-mail: [email protected] real-world social behavior during social gatherings when we Cogn Affect Behav Neurosci need to monitor the changing facial expressions of an indi- Hornak et al., 2004; McAlonan & Brown, 2003; Meunier, vidual. Animal studies have suggested that the hippocampus Bachevalier, & Mishkin, 1997; Rudebeck & Murray, 2008; disambiguates, or separates, overlapping sequences (Agster, Schoenbaum, Setlow, Nugent, Saddoris, & Gallagher, 2003; Fortin, & Eichenbaum, 2002; Bower, Euston, & McNaugh- Tsuchida, Doll, & Fellows, 2010), proactive interference ton, 2005; Ginther, Walsh, & Ramus, 2011; Wood, (Caplan, McIntosh, & De Rosa, 2007), and delayed non- Dudchenko, Robitsek, & Eichenbaum, 2000), and neuroim- match-to-sample working memory tasks involving small aging studies have shown hippocampal activation when stimulus sets (LoPresti et al., 2008; Otto & Eichenbaum, learning (Kumaran & Maguire, 2006; Shohamy & Wagner, 1992; Schon, Tinaz, Somers, & Stern, 2008). Together, the 2008) and retrieving (Brown, Ross, Keller, Hasselmo, & findings that the orbitofrontal cortex is involved in mne- Stern, 2010; Ross, Brown, & Stern, 2009) overlapping monic tasks in which interference is present and that the sequences. Additionally, neuroimaging studies (LoPresti et orbitofrontal cortex is important for processing social cues al., 2008; McIntosh, Grady, Haxby, Ungerleider, & Horwitz, suggest that the orbitofrontal cortex may interact with the 1996; Olsen et al., 2009; Ranganath, Cohen, & Brozinsky, hippocampus to create, maintain, and retrieve overlapping 2005; Ranganath & D’Esposito, 2001; Schon et al., 2005; representations of the same individual seen with multiple Schon, Hasselmo, Lopresti, Tricarico, & Stern, 2004; facial expressions in working memory. Schon, Ross, Hasselmo, & Stern, 2013; Stern, Sherman, To investigate the contributions of hippocampus and Kirchhoff, & Hasselmo, 2001), studies in patients with orbitofrontal cortex to the encoding, maintenance, and re- medial temporal lobe damage (Hannula, Tranel, & Cohen, trieval of overlapping identity information during working 2006; Hartley et al., 2007; Nichols, Kao, Verfaellie, & memory, participants performed a modified delayed match- Gabrieli, 2006; Olson, Moore, Stark, & Chatterjee, 2006; to-sample working memory task with pairs of face stimuli. Olson, Page, Moore, Chatterjee, & Verfaellie, 2006), and In the overlapping condition, participants viewed a pair of electrophysiological recordings (Axmacher, Elger, & Fell, pictures of the same individual shown with two different 2009) have suggested that the hippocampus is involved facial expressions. Importantly, the nonoverlapping condi- during the maintenance of information in working memory. tion consisted of two different faces with two different facial Together, the findings that the hippocampus is involved in expressions. After the sample phase, the participants re- working memory and during the disambiguation of membered the pair of stimuli across a short delay period. overlapping stimuli in long-term memory suggest that the At test, they indicated whether a test face matched one of the hippocampus may be involved when using social cues to sample faces shown before the delay. By comparing the disambiguate multiple presentations of the same person over overlapping and nonoverlapping conditions, the brain re- short delay periods. sponses active during the disambiguation of two In addition to the hippocampus, the orbitofrontal cortex overlapping representations of the same person encountered may also be a critical region when disambiguating two with two different facial expressions during working mem- encounters with the same individual in working memory. ory encoding, maintenance, and retrieval could be exam- The orbitofrontal cortex is central to theories of social rein- ined. We also conducted a functional connectivity analysis forcement learning (Kringelbach & Rolls, 2003; Rolls, to determine whether the orbitofrontal cortex and hippocam- 2004, 2007; Tabbert, Stark, Kirsch, & Vaitl, 2005). Impor- pus work together when disambiguating overlapping stimuli tantly, the maintenance of socially relevant information such in working memory. The results of the study provide insight as faces (Courtney, Ungerleider, Keil, & Haxby, 1996; into the brain mechanisms responsible during social situa- Haxby, Petit, Ungerleider, & Courtney, 2000; LoPresti et tions in which it is important to keep different encounters al., 2008; Sala, Rama, & Courtney, 2003) and emotional with the same individual separate. expressions (LoPresti et al., 2008) over short delays acti- vates the orbitofrontal cortex. Along with its role in process- ing social information, the orbitofrontal cortex has been Materials and method linked to the disambiguation of overlapping representations in long-term memory. In general, lateral orbitofrontal cortex Participants is more strongly functionally connected to the hippocampus when retrieving disambiguated overlapping sequences A group of 18 healthy individuals (seven male, 11 female; (Brown, Ross, Tobyne, & Stern, 2012; Ross, Sherrill, & mean age = 19.2 years, SD = 1.17 years) with no history of Stern, 2011) from long-term memory. Additionally, the neurological or psychiatric illness were recruited from the orbitofrontal cortex is critical for tasks in which interference Boston University population for this study. Their vision caused by repeated stimulus exposures must be overcome, was either normal or corrected to normal. All participants such as in reversal learning (Berlin, Rolls, & Kischka, 2004; were screened for MRI environment compatibility. Eligible Chudasama & Robbins, 2003; Fellows & Farah, 2003; individuals who agreed to participate gave signed informed Cogn Affect Behav Neurosci consent in accordance with the Human Research Committee identity. These neutral expressions were not used in the of the Massachusetts General Hospital and the Institutional scanning task. Preexposure consisted of presenting all
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