Role of the hippocampus and orbitofrontal cortex during the disambiguation of social cues in working memory

Abstract

Human social interactions are complex behaviors requiring the concerted effort of multiple neural systems to track and monitor the individuals around us. Cognitively, adjusting our behavior on the basis of changing social cues such as facial expressions relies on working memory and the ability to disambiguate, or separate, the representations of overlapping stimuli resulting from viewing the same individual with different facial expressions. We conducted an fMRI experiment examining the brain regions contributing to the encoding, maintenance, and retrieval of overlapping identity information during working memory using a delayed match-to-sample task. In the overlapping condition, two faces from the same individual with different facial expressions were presented at sample. In the nonoverlapping condition, the two sample faces were from two different individuals with different expressions. fMRI activity was assessed by contrasting the overlapping and nonoverlapping conditions at sample, delay, and test. The lateral orbitofrontal cortex showed increased fMRI signal in the overlapping condition in all three phases of the delayed match-to-sample task and increased functional connectivity with the hippocampus when encoding overlapping stimuli. The hippocampus showed increased fMRI signal at test. These data suggest that lateral orbitofrontal cortex helps encode and maintain representations of overlapping stimuli in working memory, whereas the orbitofrontal cortex and hippocampus contribute to the successful retrieval of overlapping stimuli. We suggest that the lateral orbitofrontal cortex and hippocampus play a role in encoding, maintaining, and retrieving social cues, especially when multiple interactions with an individual need to be disambiguated in a rapidly changing social context in order to make appropriate social responses.

Figure 1

Delayed match-to-sample (DMS) task showing trials where identity information was overlapping (OL) and non-overlapping (NOL). A trial consisted of 3 time-locked components: a sample period where two faces were presented sequentially for 2 seconds each, an 8 second delay period and a 2 second test period where a single face was presented. Trials were separated by 8, 10, or 12 second inter-trial intervals (ITI). During OL trials, participants were presented with a pair of sample faces from the same individual with different expressions. During NOL trials, participants were presented with a pair of sample faces from two different individuals with different expressions. In order for a trial to be a match, both the identity and facial expression of the test face had to match one of the two sample faces. Non-match trials contained test stimuli that were the same identity as one of the two sample faces, but with a different expression. The OL trial shown in the top panel is an example of a match trial, and the NOL trial (bottom panel) is an example of a non-match trial.

Figure 2

Behavioral performance during delayed match to sample task. A. Mean percent correct for overlapping (dark grey bars) and non-overlapping (light grey bars) conditions during match and non-match trials. B. Reaction times (msec) for overlapping (dark grey bars) and non-overlapping (light grey bars) conditions during match and non-match trials. * indicate significant differences between comparisons. Error bars = standard error of the mean. Significance level was set at p ≤ 0.05.

Figure 3

Statistical parametric maps showing significantly greater fMRI activity during the disambiguation of overlapping stimuli in working memory. A. fMRI activation in the orbitofrontal cortex (y = 40) related to the encoding of overlapping stimuli (OL sample > NOL sample). B. fMRI activity in the orbitofrontal cortex (y = 42) during the maintenance of overlapping stimuli across a short delay period (OL delay > NOL delay). C. Activations in orbitofrontal cortex bilaterally (OFC; yellow circles) and the right hippocampus (green circle) during the successful retrieval of overlapping stimuli in working memory (OL Match > NOL Match). Displayed slices are from y = 34. For display purposes the statistical parametric map is shown superimposed on a single participant’s anatomic image (p = 0.01 with 88 contiguous voxels). R = right hemisphere.

Figure 4

Summary of functional connectivity between lateral orbitofrontal cortex and the hippocampus, caudate and putamen regions of interest. The r value of the correlation between the orbitofrontal cortex and each region of interest for the overlapping (OL) and non-overlapping (NOL) conditions are reported. A. At sample (top), right lateral orbitofrontal-hippocampal functional connectivity at sample was stronger during the overlapping compared to the non-overlapping condition (indicated by **). The putamen and hippocampus were more strongly connected to the orbitofrontal cortex collapsing across condition (thickened arrows). At test (bottom), right lateral orbitofrontal-caudate functional connectivity was stronger during the non-overlapping condition compared to the overlapping condition (indicated by **) though the putamen showed the strongest functional connectivity with the orbitofrontal cortex when collapsing across condition (thickened arrow). B. The left lateral orbitofrontal cortex was more strongly functional connected to the putamen when collapsing across condition (thickened arrow).