Amygdala involvement in human avoidance, escape and approach behavior

Abstract

Many forms of psychopathology and substance abuse problems are characterized by chronic ritualized forms of avoidance and escape behavior that are designed to control or modify external or internal (i.e., thoughts, emotions, bodily sensations) threats. In this functional magnetic resonance imaging investigation, we examined amygdala reactivity to threatening cues when avoidance responding consistently prevented contact with an upcoming aversive event (money loss). In addition, we examined escape responding that terminated immediate escalating money loss and approach responding that produced a future money gain. Results showed cues prompting avoidance, escape and approach behavior recruited a similar fronto-striatal-parietal network. Within the amygdala, bilateral activation was observed to threatening avoidance and escape cues, even though money loss was consistently avoided, as well as to the reward cue. The magnitude of amygdala responses within subjects was relatively similar to avoidance, escape and approach cues, but considerable between-subject differences were found. The heightened amygdala response to avoidance and escape cues observed within a subset of subjects suggests threat-related responses can be maintained even when aversive events are consistently avoided, which may account for the persistence of avoidance-coping in various clinical disorders. Further assessment of the relation between amygdala reactivity and avoidance-escape behavior may prove useful in identifying individuals with or at risk for neuropsychiatric disorders.

Figure 1. Approach, avoidance and escape contingencies and associated timing parameters

The schematic shows each cue-response-outcome contingency employed and associated timing parameters. Distinct cues prompted approach responding that produced a future money gain, avoidance responding that prevented a future money loss and escape responding that terminated immediate escalating money loss. A neutral fixation cross (not shown) served as the baseline condition for imaging analyses. Pretraining using a contingency shaping procedure established stable and accurate responding during neuroimaging.

Figure 2. Amygdala activation to avoidance, escape and approach cues

Panel A highlights bilateral amygdala responses to cues that prompted avoidance, escape and approach behavior. The inserted plot highlights group mean contrast values and bars represent the standard error. Panel B presents frequency distributions of the number of subjects within a range of contrast values by condition and amygdala. Results highlight that most subjects exhibited positive contrast values and there was considerable variability between-subjects.

Figure 3. Distribution of individual subject contrast values

Individual subject contrast values highlighting the magnitude of activation observed in the left amygdala (top plot) and right amygdala (bottom plot) to cues that prompted avoidance, escape and approach responding. Data were arbitrarily ordered by escape contrast values. The distributions show within-subject amygdala responses were relatively similar across avoidance, escape and approach cues but the magnitude of response varied between subjects.

Figure 4. Relationships between amygdala responses and conditions

Panel A shows positive correlations between left and right amygdala within each condition. Panel B shows positive correlations between experimental conditions for each amygdala. Findings further highlight the consistency of within-subject amygdala responses and extent of between-subject differences.