Slow Accumulations of Neural Activities in Multiple Cortical Regions Precede Self-Initiation of Movement: An Event-Related fMRI Study

Abstract The neural processes underlying self-initiated behavior (behavior that is initiated without as external stimulus trigger) are not well understood. This event-related fMRI study investigated the neural origins of self-initiated behaviors in humans, by identifying brain regions that increased in neural activities several seconds prior to self-initiated movements. Subjects performed a hand grasping task under two conditions: a free timing and cued timing condition. The supplementary motor area (SMA) began to activate several seconds prior to self-initiated movement (accounting for hemodynamic delay), representing a potential blood oxygenation level dependent (BOLD) signal correlate of the readiness potential on electroencephalogram, referred to here as “readiness BOLD signals.” Significant readiness BOLD signals were also observed in the right frontoparietal areas, precuneus, and insula, all of which are known to contribute to internally-generated behaviors, but with no prior evidence for such early and slow accumulation of neural activities. Moreover, visual and auditory cortices also exhibited clear readiness BOLD signals with similar early onsets, even absent external stimulation. Slow accumulation of neural activities throughout distributed cortical areas, including sensory, association, and motor cortices, underlies the generation of self-initiated behaviors. These findings warrant reconsideration of the prevailing view that the SMA or some other specific locus in frontoparietal cortex serves as the ultimate neural origin of self-initiated movement. Significance Statement A stimulus can trigger a chain of neural activities that culminate in a behavior, but behaviors can also be initiated endogenously, without an external stimulus. We investigated the neural origins of self-initiated behaviors by identifying brain regions that displayed increased neural activity several seconds before onset of self-initiated movements. Our analysis revealed slow accumulation of neural activities that preceded self-initiated movements in several brain regions including the sensory, association, and motor cortices. We propose that endogenous accumulation of neural activities in networks of multiple cortical regions underlie generation of self-initiated movement.