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Review
. 2009 Nov 3;19(20):R958-62.
doi: 10.1016/j.cub.2009.08.010.

Social attention and the brain

Jeffrey T Klein  1 , Stephen V Shepherd, Michael L Platt
Affiliations
Review

Social attention and the brain

Jeffrey T Klein et al. Curr Biol. .

Abstract

Humans and other animals pay attention to other members of their groups to acquire valuable social information about them, including information about their identity, dominance, fertility, emotions, and likely intent. In primates, attention to other group members and the objects of their attention is mediated by neural circuits that transduce sensory information about others and translate that information into value signals that bias orienting. This process likely proceeds via two distinct but integrated pathways: an ancestral, subcortical route that mediates crude but fast orienting to animate objects and faces; and a more derived route involving cortical orienting circuits that mediate nuanced and context-dependent social attention.

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Figures

Figure 1
Figure 1. Connectivity of social (red), reward (blue), and orienting (green) cortical areas governing social attention
In addition to the cortical pathway, a fast subcortical pathway connects superior colliculus to amygdala via the thalamus (not shown here). Note that multiple social processing areas lie along superior temporal sulcus, occupying both posterior and anterior temporal lobe, and that functional activity in imaging tasks has not been conclusively integrated with past anatomical or electrophysiological studies. PPC, posterior parietal cortex, including macaque areas 7A and LIP; STS, superior temporal sulcus regions; SEF, supplementary eye fields; FEF, frontal eye fields; OFC, orbitofrontal cortex; AMYG, amygdala.
Figure 2
Figure 2. The LIP population response simultaneously encodes social image value and fluid value during a ‘pay-per-view’ choice task
(A) Average firing rate for 34 neurons plotted against time for all trials in which the subject chose to view the image (T2) in the neuron’s response field, separated by image class. Inset: values determined for different image classes for two male monkey subjects (open and closed bars), in ms of fluid delivery time. Positive deflections indicate the subject was willing to forgo fluid to view that image class. Negative deflections indicate the subject required fluid overpayment to choose that image class. Hindquarters refers to the perineal sexual signals of familiar females. Dominant and subordinate refer to the faces of familiar dominant and subordinate males. Gray refers to a plain gray square matched for size and luminance to the other image classes. (B) Average firing rate of the population for all trials in which the subject chose to view the image (T2) in the neuron’s response field, separated by fluid value relative to the non-chosen target (T1). (C) Firing rates plotted as a function of image value in four 200 ms epochs. Black symbols represent regressions performed on all data in which the subject chose to view the image, and gray symbols represent the same analysis restricted to trials in which the fluid payoff for choosing T1 was equal toT2. (D) Firing rates plotted as a function of the difference in fluid payoff between T2 and T1. Black symbols represent regression performed on all data in which the subject chose to view the image, and gray symbols represent the same analysis restricted to trials in which the image value calculated for that block was greater than -5 and less than 5 ms. Error bars represent SEM. The data in (C,D) were binned for display, but all regressions were performed on raw data. *p < 0.05, **p < 10 −3. (Adapted with permission from [19].)
Figure 3
Figure 3. LIP neurons mirror observed gaze
(A) Gaze following in macaques. An image of a monkey face with averted gaze (cue) was displayed centrally for 100, 200, 400 or 800 ms. Next, the cue was extinguished simultaneously with the appearance of a peripheral target located in the direction the of gaze of the cue (congruent condition) or directly opposite (incongruent condition). Monkeys then immediately shifted gaze to the peripheral target to receive a fluid reward. For cue durations≤400 ms the congruent condition elicited reaction time savings compared to the incongruent condition, indicating a shift of attention. Error bars represent SEM across sessions. (B) Neural cue responses in LIP. Significant neuronal responses to observed gaze direction in 10 ms bins. Neurons with firing rates enhanced by cues with gaze directed at their response fields (red) are temporally clustered in the time windows for which gaze-following behavior is strongest. Those neurons with firing rates suppressed by cues with gaze directed toward their response fields maintain tonic decreases in activity throughout the fixation period. (Adapted with permission from [15].)
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