Consistent with findings in non-human animals (15
), maltreated participants reported elevated depressive and anhedonic symptoms, rated reward-predicting cues less positively, and showed decreased anticipatory reward activity in the left pallidus relative to controls. Results indicate that childhood adversity that includes maltreatment is associated with impaired reward processing (13
). Furthermore, the findings highlight a neural mechanism that could contribute to relationships between childhood adversity and psychopathology: decreased anticipatory reward activity in the left basal ganglia. The pallidus integrates reward information and conveys it to motor cortex via the thalamus (44
). Thus, pallidus dysfunction might weaken the ability of reward-predicting cues to elicit goal-directed actions.
The relationship between childhood adversity and decreased subjective and neural responses to reward-predicting cues, rather than rewards themselves, was predicted based on findings in non-human animals. For example, early maternal deprivation in marmosets impaired motivation to work for liquid reinforcement but did not affect consummatory behavior (17
). We expected similar results because DA neurons that project to the basal ganglia are susceptible to stress-related dysfunction (18
) and critical for incentive motivation (21
). However, it should be noted that early adversity can also weaken the hedonic impact of obtained rewards (16
), possibly via effects on opioid systems (45
). Accordingly, group differences in consummatory responses might emerge in larger samples or different paradigms.
The findings are consistent with the hypothesis that childhood adversity may have affected the development of DA systems. However, any strong causal interpretation of the data would be premature. In this small sample, we cannot disentangle effects of maltreatment per se from many potential correlates of maltreatment, such as inherited dysfunction in neural activity, parental depression or substance abuse, or the contribution of previous psychiatric issues (). Prospective studies using larger samples are needed to distinguish among such correlated factors.
Although the SCID and CES-D revealed little evidence of current clinical depression in maltreated participants, the groups differed on self-reported symptoms of depression and anhedonia. Moreover, when MASQ-AD scores and reward cue valence ratings were controlled, the Group
effect on left pallidus reward cue responses became non-significant. One possibility is that the anhedonic symptoms and basal ganglia dysfunction are two manifestations of the same dysfunction. Indeed, MASQ-AD scores and reward cue responses in the left pallidus and left putamen were negatively correlated. In addition, the attenuated response to reward-predicting cues in the left pallidus is consistent with evidence of basal ganglia dysfunction in clinical depression. For example, relative to controls, depressed individuals showed weaker basal ganglia responses to reward-predicting cues and gains in the MID task (33
), reduced ventral striatal responses to positive words (46
), decreased caudate glucose metabolism (47
) and blood flow (48
), and reduced extracellular caudate and putamen DA (49
The restriction of deficits to the left hemisphere was not predicted but echoes reports that post-stroke depression more often follows damage to the left versus right hemisphere (50
), with globus pallidus lesions highly predictive of depression (51
). Moreover, a study in healthy participants reported a positive correlation between D2-receptor availability in the left putamen and incentive motivation (52
), consistent with the fact that left hemisphere group differences were specific to reward anticipation. Findings are also consistent with reported relationships between childhood maltreatment and electrophysiological abnormalities over the left hemisphere (53
). The reason for this hemispheric asymmetry is unclear, but asymmetrical projections of DA neurons may play a role (54
Critically, results do not reflect a global deficit in maltreated participants. There were no significant group differences in affective ratings to any stimulus except reward cues, and no differences in basal ganglia response to (a) loss or no-incentive cues in the left hemisphere, (b) any cue in the right hemisphere, or (c) any outcome. Furthermore, group differences in left pallidus reward cue responses remained after controlling for anxiety and general distress ().
The study possesses several limitations. First, several maltreated individuals were excluded due to active substance abuse, and the striatum is tonically hypoactive in substance abusers (55
). Thus, we may have excluded individuals with severe reward processing dysfunction, yielding a conservative estimate of effects of maltreatment on reward processing. Second, the lack of group differences in response to loss cues and penalties may reflect a weakness of the MID task: because participants knew they would be paid for participation, the loss cues and penalties may not have been sufficiently aversive to elicit group differences. Notably, other studies report relationships between childhood adversity and sensitivity to emotionally negative stimuli (e.g., 56
). Third, the current sample was too small to determine whether a dose-response relationship exists between extent or age of onset of maltreatment and responses to reward cues, or to examine whether specific types of maltreatment have different effects on reward processing. Larger studies are needed to address these issues, and to investigate whether particular genetic backgrounds or social supports can protect reward systems from adversity-induced dysfunction (57
Fourth, because controls and maltreated participants were from different cohorts, variables besides maltreatment may have affected the results. Three considerations mitigate this concern. First, the loss and no-incentive conditions and cue/outcome design served as internal controls that allowed us to pinpoint the predicted differences in reward anticipation; the lack of differences in other conditions argues against a general deficit in maltreated participants. Second, the strong basal ganglia response to reward cues demonstrated by the controls is the norm in the MID task and has been demonstrated in samples differing in age, education, and sociodemographics (22
). Thus, the findings reflect a deficit in maltreated participants rather than atypical results in the controls. Third, Group
predicted left pallidus reward cue responses after adjusting for age, education, anxiety, and basal ganglia volumes. Nonetheless, groups may have differed on other variables not measured, especially because maltreated individuals tend to be exposed to multiple forms of childhood adversity (59
). Consequently, results should be interpreted in terms of childhood adversity, rather than maltreatment per se