Parsing Reward Processing Substages With Multimodal EEG-fMRI

Multimodal imaging studies that combine temporally and spatially precise methods can enhance understanding of reward neurocircuitry by revealing how signals specifically time-locked to reward processing substages relate to functional network-level activity. Prior reward studies that require decision making and/or motor responses to obtain rewards may complicate efforts to isolate basic reward responses from higher-order functions that support reward attainment. Here, we take an integrated, multimodal approach to evaluate anticipatory and consummatory reward processing substages, while minimizing demands on higher-order cognitive and motor processes. Functional magnetic resonance imaging (fMRI) and electrophysiological (EEG) data were separately recorded from 52 adults playing a simple, slot machine task, with reward outcomes independent of performance. Joint Independent Component Analyses (jICAs) were conducted with EEG-based event-related potential (ERP) difference waveforms and fMRI contrast images specific to reward anticipation and outcome processing substages. Resulting joint independent components (JICs) segregated reward processing substages, indicating significant co-modulation between temporal ERP and spatial fMRI signals (p < 0.001). During Reward Anticipation, a JIC with the temporal signature of the stimulus preceding negativity (SPN) ERP component covaried with fMRI activation in bilateral supplementary motor areas (pre-SMA/SMA) and inferior fronto-insular salience network regions implicated in attentional orienting and shifting. During Reward Feedback, JICs with the temporal signature of the reward positivity (RewP) ERP component covaried with fMRI activation in dorsal anterior cingulate cortex (dACC), ventral striatum, SMA, and inferior frontal cortex, extending to the insula. Further, trait reward sensitivity correlated with jICA-informed Win > Loss brain activations during Reward Feedback (p = 0.016). Our findings demonstrate that temporally precise electrophysiological and spatially rich hemodynamic measures of reward processing converge to map onto specific substages of reward-related brain processes. ERP and fMRI signaling during reward feedback support covariation of the RewP with dACC-striatal reward networks while the SPN covaried with fMRI signal in pre-SMA/SMA and inferior fronto-insular regions implicated in motor planning, salience, and attention.