The nucleus accumbens is involved in both the pursuit of social reward and the avoidance of social punishment

Abstract

Human social motivation is characterized by the pursuit of social reward and the avoidance of social punishment. The ventral striatum/nucleus accumbens (VS/Nacc), in particular, has been implicated in the reward component of social motivation, i.e., the 'wanting' of social incentives like approval. However, it is unclear to what extent the VS/Nacc is involved in avoiding social punishment like disapproval, an intrinsically pleasant outcome. Thus, we conducted an event-related functional magnetic resonance imaging (fMRI) study using a social incentive delay task with dynamic video stimuli instead of static pictures as social incentives in order to examine participants' motivation for social reward gain and social punishment avoidance. As predicted, the anticipation of avoidable social punishment (i.e., disapproval) recruited the VS/Nacc in a manner that was similar to VS/Nacc activation observed during the anticipation of social reward gain (i.e., approval). Stronger VS/Nacc activity was accompanied by faster reaction times of the participants to obtain those desired outcomes. This data support the assumption that dynamic social incentives elicit robust VS/Nacc activity, which likely reflects motivation to obtain social reward and to avoid social punishment. Clinical implications regarding the involvement of the VS/Nacc in social motivation dysfunction in autism and social phobia are discussed.

Keywords: Avoidance; Motivation; Nucleus accumbens; Social punishment; Social reward; Ventral striatum.

Fig.1

Illustration of the social incentive delay task including two different task versions: (1) seeking social approval (APR), and (2) avoiding social disapproval (AVOI). Each task comprised a total of 48 incentive trials and 48 control trials (in addition to null events) presented across six runs in total, three for each task type, with intermixed incentive and control trials in each run. To increase the ecological validity of the paradigm, static photos were replaced with short movie clips of actors expressing facial expressions along with other nonverbal gestures (see text for more details).

Fig.2

(A) Reaction times for hits (in msec) for the control and incentive conditions separately for the two social reward tasks. Participants responded faster during incentive trials relative to the control trials, with generally shorter RTs observed in the AVOI task than the APR task. A significant interaction effect emerged, indicating that participants decreased response speed to potential reward versus control more strongly when approval was at stake than under conditions of avoiding disapproval. (B) and (C) Mean parameter estimates extracted from our a priori ROIs – the left and right Nacc – during the anticipation phase (between cue onset and feedback onset) separately for the two social tasks. When entered into a repeated-measures ANOVA with task (APR, AVOI), trial (incentive, control) and hemisphere (left, right) as the within-subjects factors, a main effect of trial type (F (1, 21) = 7.67, p = 0.012, η²_p = 0.27) and a trial by site interaction effect (F (1, 21) = 7.93, p = 0.010,,η²_p = 0.27) emerged, reflecting greater Nacc activation for anticipated social approval and avoidance of disapproval versus control, particularly in the right hemisphere (right: p = 0.003; left: p = 0.068). The negative parameter estimates for control trials, particularly in the APR task, suggest that the non-incentive control trials might have been experienced as reward ‘omission’ leading to decreased activation in VS/Nacc. Error bars indicate ± 1.0 SEM.

Fig.3

Results of the whole-brain analyses for the two high-level anticipation contrasts (APR>CON and AVOI>CON) revealed significant activation in a cluster comprising ventral and dorsal striatum as well as thalamus. No significant activation differences were found when the two contrasts were compared against each other. Z scores are based on cluster-level correction for multiple comparisons across the whole brain with a mean cluster threshold of Z > 2.3 and a cluster-corrected significance threshold of p ≤ 0.05 using Gaussian random field theory (sagittal slices).

Fig.4

To test our a priori hypothesis of greater signal changes in the Nacc during anticipated approval and avoidance of disapproval versus anticipated non-incentive control, we performed ROI analyses within bilateral Nacc for the contrasts APR>CON and AVOI>CON as well as for APR and AVOI combined vs. CON. The Nacc was anatomically defined based on the Harvard-Oxford structural probabilistic atlas. (A) Both social incentive conditions together revealed the expected strong bilateral Nacc activation (hot colors). (B) Results separately for the two contrasts of interest (i.e., APR>CON, AVOI>CON) showed that the prospect of avoiding social punishment (i.e., disapproval; hot colors) recruited the Nacc in a manner that was similar to Nacc activation during the seeking of social reward (i.e., approval; cool colors), particularly in the right hemisphere. ROI results are family wise error (FWE) corrected at p ≤ 0.05 (coronal slice).