Elevated pre-supplementary motor area activity during reward expectancy: An impulsivity-related neural marker of vulnerability to bipolar and externalizing disorders

Mania/hypomania is pathognomonic of bipolar disorder (BD), yet early identification remains challenging. Impulsivity is a key feature of mania/hypomania and of externalizing disorders that may predispose to BD, but neural markers of impulsivity-related risk remain unknown. This study aimed to identify reward expectancy (RE)-related neural correlates of impulsivity facets, test moderation by current affective/anxiety symptoms, and determine whether such markers differentiate BD and/or externalizing disorders from low impulsivity individuals. Two independent BD-risk samples aged 18–30 years, including individuals with prior externalizing disorder diagnoses but not BD, were recruited; a euthymic BD group was also recruited. Impulsivity facets were assessed via Behavioral Activation System (BAS) and UPPS-P scales. Whole-brain regressions identified neural correlates of impulsivity facets during RE. Linear models tested replication and current affective/anxiety symptom moderation. ANCOVA compared neural activity among BD, externalizing, and non-BD/externalizing impulsivity tertile groups. Whole-brain regressions revealed a positive association between BAS Fun Seeking and pre-supplementary motor area (pre-SMA) activity ( p FWE = 0.003, k = 167), which replicated when depressive symptoms were covaried (discovery: β = 2.73, p < 0.001; replication: β = 0.88, p = 0.036; combined: β = 1.49, p < 0.001). A significant pre-SMA × depression interaction ( β = –0.08, p = 0.037) indicated depressive symptoms attenuated the pre-SMA-Fun Seeking association. Group comparisons revealed greater pre-SMA activity in high-Fun Seeking ( p < 0.001) and externalizing disorder groups ( p = 0.039) versus low-Fun Seeking, with similar trends observed in BD once individuals taking medications, particularly benzodiazepines ( p = 0.012), were excluded. Pre-SMA hyperactivity during RE is a robust neural correlate of BAS Fun Seeking, moderated by depression severity. This pattern represents a trait-linked neural marker of impulsivity associated with vulnerability to BD and externalizing disorders, informing early risk identification and intervention.