TY - JOUR
T1 - Ventromedial prefrontal value signals and functional connectivity during decision-making in suicidal behavior and impulsivity
AU - Brown, Vanessa M.
AU - Wilson, Jonathan
AU - Hallquist, Michael N.
AU - Szanto, Katalin
AU - Dombrovski, Alexandre Y.
N1 - Funding Information:
This work was funded by the National Institutes of Health, Bethesda, MD, USA (R01MH100095 and R01MH048463 to AYD; K01MH097091 to MNH; R01MH085651 to KS; and T32MH019986 to VMB). The funding agency had no role in the design and conduct of the study; the collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; or decision to submit the manuscript for publication. The authors do not have any conflicts of interest to disclose.
Publisher Copyright:
© 2020, The Author(s).
PY - 2020/5/1
Y1 - 2020/5/1
N2 - 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.
AB - 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.
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U2 - 10.1038/s41386-020-0632-0
DO - 10.1038/s41386-020-0632-0
M3 - Article
C2 - 32035425
AN - SCOPUS:85079718074
SN - 0893-133X
VL - 45
SP - 1034
EP - 1041
JO - Neuropsychopharmacology
JF - Neuropsychopharmacology
IS - 6
ER -