Working memory for social cues recruits orbitofrontal cortex and amygdala: a functional magnetic resonance imaging study of delayed matching to sample for emotional expressions

Abstract

During everyday interactions, we continuously monitor and maintain information about different individuals and their changing emotions in memory. Yet to date, working memory (WM) studies have primarily focused on mechanisms for maintaining face identity, but not emotional expression, and studies investigating the neural basis of emotion have focused on transient activity, not delay related activity. The goal of this functional magnetic resonance imaging study was to investigate WM for two critical social cues: identity and emotion. Subjects performed a delayed match-to-sample task that required them to match either the emotional expression or the identity of a face after a 10 s delay. Neuroanatomically, our predictions focused on the orbitofrontal cortex (OFC) and the amygdala, as these regions have previously been implicated in emotional processing and long-term memory, and studies have demonstrated sustained OFC and medial temporal lobe activity during visual WM. Consistent with previous studies, transient activity during the sample period representing emotion and identity was found in the superior temporal sulcus and inferior occipital cortex, respectively. Sustained delay-period activity was evident in OFC, amygdala, and hippocampus, for both emotion and identity trials. These results suggest that, although initial processing of emotion and identity is accomplished in anatomically segregated temporal and occipital regions, sustained delay related memory for these two critical features is held by the OFC, amygdala and hippocampus. These regions share rich connections, and have been shown previously to be necessary for binding features together in long-term memory. Our results suggest a role for these regions in active maintenance as well.

Figure 1.

DMS and CON task. In all tasks, a trial consisted of three time-locked components: a 2 s face presentation (sample), followed by a 10 s delay period, and by a 2 s face presentation (test). Trials were separated by a variable-length ITI. During EMO_DMS trials, subjects matched the emotional expression of the face, and facial identity was irrelevant. During ID_DMS trails, subjects matched the identity of the face and the emotional expression was irrelevant. In the case of an EMO-match trial (top), the test face showed the same emotional expression as the one shown by the sample face, but was from a different actor. In the case of an ID-match trial (middle), the test face was from the same actor as that seen during the sample phase, but showed a different emotional expression. During CON trials (bottom), Fourier phase scrambled versions of the face stimuli were presented and subjects were instructed to respond to the number presented in the center of the test stimulus.

Figure 2.

Multiple regression analysis. A, Stick functions were used to create six contrasts for comparison of DMS and CON task components. S, Sample; D, delay; T, test. Regressors 2 and 6 were used to assess activity related to face processing and active maintenance, respectively. Bars indicate the positioning of the HRF. Stick functions for delay periods were divided into five bars spread across the five TRs of the delay to account for the sustained time course of the delay period activity (Schluppeck et al., 2006). B, Example of regressors created by convolving the six stick contrasts with a gamma-variate function (HRF) (Boynton et al., 1996). The bottom graph shows all six regressors together.

Figure 3.

Sustained delay period activity in orbitofrontal cortex. A, fMRI results from the active maintenance analysis (regressor 6) demonstrating sustained activity in left OFC, x = −46, y = 26, z = −6 (arrows). Statistical parametric maps are shown superimposed onto the canonical average T1-weighted MNI brain. B, Sustained activity is displayed in the line graph representing the signal intensity time course extracted from suprathreshold voxels within a 5 mm sphere surrounding the ROIs peak activation (green, DMS trials; gray, CON trials). Blue and red horizontal bars indicate time points when sample and test faces were presented and the intervening delay period, respectively. Shaded areas indicate time points that were averaged to obtain signal amplitudes for sample, delay, and test components of the task. C, Transient dissociation between EMO and ID tasks in OFC. Greater activity was found for EMO than ID during sample face presentations. In contrast, significant delay period activity was similar for EMO and ID tasks. The bar graph represents signal difference values (DMS − CON) for sample, delay, and test. Signal intensity values for CON trials were subtracted from corresponding values for DMS trials to compute a signal difference value for each task component. D, Greater OFC activity at test for EMO_DMS trials with negative valence. During test phase face presentations within EMO trials, negatively valenced faces elicited a significantly greater signal than positively valenced faces. L, Left; R, right. Error bars indicate SEM. Asterisks indicate significant difference.

Figure 4.

Sustained delay period activity in medial temporal lobe structures. A, Left amygdala, x = −18, y = −4, z = −20 (arrows). B, Left mid-hippocampal body, x = −32, y = −30, z = −8 (arrows). Statistical parametric maps are shown superimposed onto the canonical average T1-weighted MNI brain. Sustained activity is displayed in the line graphs representing signal intensity time courses extracted from suprathreshold voxels within a 5 mm sphere surrounding the ROIs peak activation (green, DMS trials; gray, CON trials). Blue and red horizontal bars indicate time points when sample and test faces were presented and the intervening delay period, respectively. Shaded areas indicate time points that were averaged to obtain signal amplitudes for sample, delay, and test components of the task. Bar graphs represent signal difference values (DMS − CON) for sample, delay, and test. Signal intensity values for CON trials were subtracted from corresponding values for DMS trials to compute a signal difference value for each task component. Significant delay period activity was similar for EMO and ID tasks in amygdala and hippocampus ROIs. L, Left; R, right. Error bars indicate SEM.

Figure 5.

fMRI results from face processing analysis (regressor 2) demonstrating transient activity that is modulated by task. A, Right inferior occipital cortex, x = 50, y = −74, z = −14 (arrows). B, Right superior temporal sulcus, x = 50, y = −36, z = 0 (arrows). C, Right posterior parahippocampal cortex, x = 16, y = −36, z = −6 (arrows). Statistical parametric maps are shown superimposed onto the canonical average T1-weighted MNI brain. Line graphs represent signal intensity time courses extracted from suprathreshold voxels within a 5 mm sphere surrounding the ROIs peak activation (green, DMS trials; gray, CON trials). Blue and red horizontal bars indicate time points when sample and test faces were presented and the intervening delay period, respectively. Shaded areas indicate time points that were averaged to obtain signal amplitudes for sample, delay, and test components of the task. Bar graphs represent signal difference values (DMS − CON) for sample, delay, and test. Signal intensity values for CON trials were subtracted from corresponding values for DMS trials to compute a signal difference value for each task component. A, Greater activity for ID than EMO during sample face presentations in the right inferior occipital cortex. B, Greater activity for EMO than ID during sample face presentations in the right STS. C, Greater activity for EMO than ID during test face presentations in right parahippocampal cortex. L, Left; R, right. Error bars indicate SEM. Asterisks indicate significant difference.