Visuokinesthetic Perception of Hand Movement is Mediated by Cerebro–Cerebellar Interaction between the Left Cerebellum and Right Parietal Cortex

Abstract

Combination of visual and kinesthetic information is essential to perceive bodily movements. We conducted behavioral and functional magnetic resonance imaging experiments to investigate the neuronal correlates of visuokinesthetic combination in perception of hand movement. Participants experienced illusory flexion movement of their hand elicited by tendon vibration while they viewed video-recorded flexion (congruent: CONG) or extension (incongruent: INCONG) motions of their hand. The amount of illusory experience was graded by the visual velocities only when visual information regarding hand motion was concordant with kinesthetic information (CONG). The left posterolateral cerebellum was specifically recruited under the CONG, and this left cerebellar activation was consistent for both left and right hands. The left cerebellar activity reflected the participants' intensity of illusory hand movement under the CONG, and we further showed that coupling of activity between the left cerebellum and the “right” parietal cortex emerges during this visuokinesthetic combination/perception. The “left” cerebellum, working with the anatomically connected high-order bodily region of the “right” parietal cortex, participates in online combination of exteroceptive (vision) and interoceptive (kinesthesia) information to perceive hand movement. The cerebro–cerebellar interaction may underlie updating of one's “body image,” when perceiving bodily movement from visual and kinesthetic information.

Does vibration-induced kinesthetic illusion accompany motor responses in agonistic and antagonistic muscles?

“…Vivid movement illusion is believed to occur when about 70-90 Hz vibration is applied to the skin over the tendon 5,12,13,19,20) , unless the two antagonistic muscle groups are simultaneously vibrated at the same frequency 12) . The frequency of tendon vibration to one muscle did not differ between studies of movement illusion with 12,13) or without 17) accompanying motor responses.…”

“…In a series of studies examining whether the muscle spindle contributed to kinesthetic sensation, low-amplitude tendon vibration was used to elicit movement sensations, because the muscle spindle afferents are sensitive to low-amplitude tendon vibration between 0.2 and 1.5 mm 5,6,21) . Conversely, Naito and colleagues 17,19,20) used relatively high-amplitude tendon vibration between 2.0 and 7.0 mm at frequencies above 70 Hz. Since a smaller amplitude vibration at a constant frequency led to illusory sensation at a lower movement velocity 22) , high-amplitude tendon vibration could more easily elicit vivid movement sensations without any actual movement in the same direction, as illusory sensation is not induced by AVR.…”

“…The authors who used high-amplitude tendon vibration on subjects who experienced illusory movement sensations without muscle responses, however, carefully applied vibration with a light pressure on the surface of the skin over the tendon 17,19,20) . Eklund applied the vibration to the tendon of the knee extensors, and noted that "in order to elicit a TVR, a vibrator was fastened with strong rubber bands over the patellar ligament, or, if this placement evoked too strong a contraction, just proximal to the patella, which is somewhat less effective in eliciting TVR in the knee extensors" 3) .…”

“…Visual information on the static 20) or moving 23,25) limb would overpower kinesthetic sensations evoked by proprioceptive inputs during vibration, and kinesthetic sensations would be attenuated accordingly. Interestingly, Lackner 26) reported that, in a lighted room, subjects experienced a dissociation between the visual and proprioceptual location of their vibrated limb.…”

“…For example, when the subject tried to fix a visible finger or hand, tendon vibration of the biceps muscle elicited a kinesthetic sensation of hand movement in association with illusory elbow flexion, even though the subject did not see movement. Although movement illusion often disappeared when subjects could see their vibrated limb 14) , kinesthetic sensations were not canceled out, but only modified by the integration of visual and proprioceptive information 20,26) . Even when subjects could view their vibrated limb, they felt vivid movement sensations in the absence of notable EMG activities (TVR and AVR), correlated with the strength of the movement illusion 23) .…”