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The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys - PubMed

  • ️Wed Jan 01 2020

The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys

Benjamin M Basile et al. PLoS Biol. 2020.

Abstract

A key feature of most social relationships is that we like seeing good things happen to others. Research has implicated the anterior cingulate cortex (ACC) in attaching value to social outcomes. For example, single neurons in macaque ACC selectively code reward delivery to the self, a partner, both monkeys, or neither monkey. Here, we assessed whether the ACC's contribution to social cognition is causal by testing rhesus monkeys (Macaca mulatta) on a vicarious reinforcement task before and after they sustained ACC lesions. Prior to surgery, actors learned that 3 different visual cues mapped onto 3 distinct reward outcomes: to self ("Self"), to the other monkey ("Other"), or to neither monkey ("Neither"). On each trial, actors saw a cue that predicted one of the 3 juice offers and could accept the offer by making a saccade to a peripheral target or reject the offer by breaking fixation. Preoperatively, all 6 actors displayed prosocial preferences, indicated by their greater tendency to give reward to Other relative to Neither. Half then received selective, bilateral, excitotoxic lesions of the ACC, and the other half served as unoperated controls. After surgery, all monkeys retained the social preferences they had demonstrated with the preoperatively learned cues, but this preference was reduced in the monkeys with ACC lesions. Critically, none of the monkeys in the ACC lesion group acquired social preferences with a new set of cues introduced after surgery. These data indicate that the primate ACC is necessary for acquisition of prosocial preferences from vicarious reinforcement.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Monkeys completed a social vicarious reinforcement test before and after selective ACC damage.

(A) Top-down schematic of the test arrangement with the actor monkey facing an LCD screen next to a recipient. (B) Schematic side view of juice delivery to recipient or juice collection cylinder in Social and Nonsocial sessions. (C) Stimuli used in the Social and Nonsocial sessions in the preoperative test, postoperative retention test, and postoperative acquisition test. The cues used for fixation were rotated to create the 3 reward conditions. (D) Schematic of the trial progression in a Social session in which the stimulus signals that “reward to self” is on offer. If the monkey completed the saccade to the peripheral target, the reward condition on offer for that trial was implemented. Note that the white peripheral saccade target appeared equally often in one of 8 locations equidistant from the center. (E) Diagram of the intended lesion in sagittal and coronal views (left) and postoperative edema (white hypersignal) observed in a T2-weighted MR scan in one monkey in the ACC lesion group. MR images from all monkeys with ACC lesions available in S1 Fig. ACC, anterior cingulate cortex; ITI, intertrial interval; LCD, liquid crystal display; MR, magnetic resonance.

Fig 2
Fig 2. ACC damage reduced preoperatively learned social preferences and eliminated formation of postoperative social preferences.

(A) Prosocial preference measured as the proportion of Other trials completed minus the proportion of Neither trials completed. Positive values indicate prosocial preferences, and negative values indicate antisocial preferences. Bars show group means, and points show scores of individual monkeys (±SEM) for the preoperative baseline preference (light grey), the postoperative retention test with the preoperatively learned cues (medium grey), and the postoperative acquisition test with novel cues (dark grey). Closed symbols indicate monkeys with a significant prosocial preference, and open symbols indicate monkeys with no significant preference. (B) Trial completion rates for postoperative acquisition sessions. Proportion of trials completed for all 40 acquisition sessions as a function of trial type. Black circles = Self. Dark squares = Other. Light triangles = Neither. Each panel shows scores of one monkey, with the control monkeys on the left (C1–C3) and the lesion monkeys on the right (A1–A3). The final 20 sessions (i.e., sessions 21–40) correspond to the data depicted in panel A; the difference between Other and Neither is highlighted for those sessions. Underlying data can be found in S1 Data. ACC, anterior cingulate cortex; CON, control group.

Fig 3
Fig 3. Monkeys without prosocial preferences after ACC lesions still showed pupil size differences on Other versus Neither trials.

Difference in mean pupil change from baseline (Z score ± 95% CI) between Other and Neither trials during the 50-ms epoch fixating on the peripheral saccade target prior to juice delivery in Other and Neither trials. Positive values indicate larger pupils on Other trials, and negative values indicate larger pupils on Neither trials. Data are from the final 20 sessions of postoperative acquisition, Social condition only. Control monkeys: C1–C3; monkeys with ACC lesions: A1–A3. See also S3 Fig for the pupil widths in Other and Neither trials that went into this difference score. Underlying data can be found in S2 Data. ACC, anterior cingulate cortex.

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