Movement Initiation-Locked Activity of the Anterior Putamen Predicts Future Movement Instability in Periodic Bimanual Movement

Abstract

In periodic bimanual movements, anti-phase-coordinated patterns often change into in-phase patterns suddenly and involuntarily. Because behavior in the initial period of a sequence of cycles often does not show any obvious errors, it is difficult to predict subsequent movement errors in the later period of the cyclical sequence. Here, we evaluated performance in the later period of the cyclical sequence of bimanual periodic movements using human brain activity measured with functional magnetic resonance imaging as well as using initial movement features. Eighteen subjects performed a 30 s bimanual finger-tapping task. We calculated differences in initiationlocked transient brain activity between antiphase and in-phase tapping conditions. Correlation analysis revealed that the difference in the anterior putamen activity during antiphase compared within-phase tapping conditions was strongly correlated with future instability as measured by the mean absolute deviation of the left-hand intertap interval during antiphase movements relative to in-phase movements (r ϭ 0.81). Among the initial movement features we measured, only the number of taps to establish the antiphase movement pattern exhibited a significant correlation. However, the correlation efficient of 0.60 was not high enough to predict the characteristics of subsequent movement. There was no significant correlation between putamen activity and initial movement features. It is likely that initiating unskilled difficult movements requires increased anterior putamen activity, and this activity increase may facilitate the initiation of movement via the basal ganglia-thalamocortical circuit. Our results suggest that initiation-locked transient activity of the anterior putamen can be used to predict future motor performance.

Attention-Deficit/Hyperactivity Disorder Symptoms Coincide With Altered Striatal Connectivity

“…However, recent evidence suggests that putamen and caudate may be functionally segregated into smaller sub-regions (1, 30). The putamen is considered to consist of an anterior region, connected to pre-supplementary motor area and ACC, and a posterior region, connected to primary and secondary motor areas (2, 31, 32). Anterior putamen has been associated with higher-order cognitive aspects of motor control such as learning new movements (31), while posterior putamen has been related to execution of skilled movements (32).…”

“…The putamen is considered to consist of an anterior region, connected to pre-supplementary motor area and ACC, and a posterior region, connected to primary and secondary motor areas (2, 31, 32). Anterior putamen has been associated with higher-order cognitive aspects of motor control such as learning new movements (31), while posterior putamen has been related to execution of skilled movements (32). A functional segregation of the caudate into a dorsal and ventral region has also been suggested (1, 33).…”

Tactile sensing system including bidirectionality and enhancement of haptic perception by tactile feedback to distant part

“…In addition, use of both hands for the forceps (the tactile sensor) and the tactile display and the attention to the hand with the forceps might have relations with the enhancing effect. For bimanual action, it is known that tendency of the central nervous system attempts to synchronize the left and right side limbs [22]. In the rubber hand illusion, the temporal and spatial relationship in stimuli between the real hand and the rubber hand are important to make the illusion to be strong [23].…”

Aberrant local striatal functional connectivity in attention‐deficit/hyperactivity disorder

“…Finally, putamen regulates motor function through connections with motor cortices (Alexander et al, 1986). In addition, it is hypothesized that putamen can be subdivided into a functionally distinct anterior and posterior region (Aramaki, Haruno, Osu, & Sadato, 2011;Tricomi, Balleine, & O'Doherty, 2009). Anterior putamen has been associated with higher order cognitive aspects of motor control including learning and initiating new movements (Aramaki et al, 2011), through connections with presupplementary motor area and ACC (Helmich et al, 2010).…”

“…In addition, it is hypothesized that putamen can be subdivided into a functionally distinct anterior and posterior region (Aramaki, Haruno, Osu, & Sadato, 2011;Tricomi, Balleine, & O'Doherty, 2009). Anterior putamen has been associated with higher order cognitive aspects of motor control including learning and initiating new movements (Aramaki et al, 2011), through connections with presupplementary motor area and ACC (Helmich et al, 2010). Posterior putamen has been related to the execution of well-learnt, skilled movements (Tricomi et al, 2009), via connections to primary and secondary motor areas (Helmich et al, 2010).…”