Ventromedial prefrontal value signals and functional connectivity during decision-making in suicidal behavior and impulsivity

Suicide is linked to impaired value-based decision-making and impulsivity, but whether these risk factors share neural underpinnings is unclear. Disrupted ventromedial prefrontal cortex (vmPFC) value signals may underlie this behavioral phenotype. We investigated vmPFC value signals, vmPFC-frontoparietal connectivity, and the impact of impulsivity during decision-making in depressed individuals with and without suicidal behavior. Middle-aged and older adults (n = 116; 35 with a history of suicide attempts, 25 with ideation only, 25 depressed controls with no ideation, and 31 nonpsychiatric controls) completed a decision-making task with drifting reward probabilities during fMRI. Values of choices, estimated by a reinforcement learning model, were regressed against BOLD signal. VmPFC value activation was compared between groups. Moderating effects of impulsivity on vmPFC-frontoparietal connectivity were assessed in nonpsychiatric controls and compared among patient groups. VmPFC value responses in participants with a history of suicide attempts were reduced relative to nonpsychiatric controls (p < 0.05). In nonpsychiatric controls, vmPFC-frontoparietal connectivity was negatively moderated by impulsivity (PFWE corrected < 0.05). This effect was preserved in comparison patient groups but abolished in suicide attempters (p < 0.001). This change in neural connectivity patterns also affected behavior: people with a history of suicide attempts showed a disrupted effect of vmPFC-frontoparietal connectivity, impulsivity, and reinforcement on choice quality (p < 0.001). These effects were specific to vmPFC and not to striatum. In summary, findings from this study largely support disrupted vmPFC value signals in suicidal behavior. In addition, it uncovers an altered pattern of vmPFC-frontoparietal connectivity in impulsive people with suicidal behavior, which may underlie disrupted choice processes in a suicidal crisis.

Vanessa M. Brown, Jonathan Wilson, Michael N. Hallquist, Katalin Szanto, Alexandre Y. Dombrovski