Correlated spontaneous activity in the resting brain is increasingly recognized as a useful index for inferring underlying functional-anatomic architecture. However, despite efforts for comparison with anatomical connectivity, neuronal origin of intrinsic functional connectivity (inFC) remains unclear. Conceptually, the source of inFC could be decomposed into causal components that reflect the efficacy of synaptic interactions and other components mediated by collective network dynamics (e.g., synchronization). To dissociate these components, it is useful to introduce another connectivity measure such as effective connectivity, which is a quantitative measure of causal interactions. Here, we present a direct comparison of inFC against emEC (effective connectivity probed with electrical microstimulation [EM]) in the somatosensory system of macaque monkeys. Simultaneous EM and functional magnetic resonance imaging revealed strong emEC in several brain regions in a manner consistent with the anatomy of somatosensory system. Direct comparison of inFC and emEC revealed colocalization and overall positive correlation within the stimulated hemisphere. Interestingly, we found characteristic differences between inFC and emEC in their interhemispheric patterns. Our results suggest that intrahemispheric inFC reflects the efficacy of causal interactions, whereas interhemispheric inFC may arise from interactions akin to network-level synchronization that is not captured by emEC.