Distortion of Visuo-Motor Temporal Integration in Apraxia: Evidence From Delayed Visual Feedback Detection Tasks and Voxel-Based Lesion-Symptom Mapping

Abstract

Limb apraxia is a higher brain dysfunction that typically occurs after left hemispheric stroke and its cause cannot be explained by sensory disturbance or motor paralysis. The comparison of motor signals and visual feedback to generate errors, i.e., visuo-motor integration, is important in motor control and motor learning, which may be impaired in apraxia. However, in apraxia after stroke, it is unknown whether there is a specific deficit in visuo-motor temporal integration compared to visuo-tactile and visuo-proprioceptive temporal integration. We examined the precision of visuo-motor temporal integration and sensory-sensory (visuo-tactile and visuo-proprioception) temporal integration in apraxia after stroke by using a delayed visual feedback detection task with three different conditions (tactile, passive movement, and active movement). The delay detection threshold and the probability curve for delay detection obtained in this task were quantitative indicators of the respective temporal integration functions. In addition, we performed subtraction and voxel-based lesion-symptom mapping to identify the brain lesions responsible for apraxia and deficits in visuo-motor temporal integration. The behavioral experiments showed that the delay detection threshold was extended and that the probability curve for delay detection was less steep in apraxic patients compared to controls (pseudo-apraxic patients and unaffected patients), only for the active movement condition, and not for the tactile and passive movement conditions. Furthermore, the severity of apraxia was significantly correlated with the delay detection threshold and the steepness of the probability curve in the active movement condition. These results indicated that multisensory (i.e., visual, tactile, and proprioception) feedback was normally temporally integrated, but motor prediction and visual feedback were not correctly temporally integrated in apraxic patients. That is, apraxic patients had difficulties with visuo-motor temporal integration. Lesion analyses revealed that both apraxia and the distortion of visuo-motor temporal integration were associated with lesions in the fronto-parietal motor network, including the left inferior parietal lobule and left inferior frontal gyrus. We suppose that damage to the left inferior fronto-parietal network could cause deficits in motor prediction for visuo-motor temporal integration, but not for sensory-sensory (visuo-tactile and visuo-proprioception) temporal integration, leading to the distortion of visuo-motor temporal integration in patients with apraxia.

Stochastic resonance improves visuomotor temporal integration in healthy young adults

“…The participant was instructed to observe the reflection in the mirror with the following instruction: “Please observe your own hand reflected in the mirror.” Subsequently, the participant opened and closed their hand once, in a continuous and smooth manner, according to their own volition, after the experimenter had informed them orally that the trial had started. The self-generated movements were observed under the following 15 delay conditions using a video delay-inserting device: 33, 67, 100, 133, 167, 200, 233, 267, 300, 333, 367, 400, 433, 467, and 500 ms. As with previous studies [45–47, 75–77], this task did not include a 0 ms delay, i.e., no delay condition. During the delayed visual feedback detection task, the participant only looked at the reflection of their hand in the mirror, and not their real hand.…”

“…On the other hand, visuomotor temporal integration is an important function for hand motor control [43–47]. More specifically, it is largely supported by a neural mechanism known as the forward model [48, 49].…”

“…Therefore, comparing motor signals and visual feedback to generate temporal errors, i.e., visuomotor temporal integration, is important for hand motor control. In fact, in children with a developmental coordination disorder and adults with limb-apraxia after stroke have deficits in visuomotor temporal integration [45, 47]. In addition, the degree of deficiency in visuomotor temporal integration correlates significantly with the severity of the movement disorder [45–47].…”

“…In fact, in children with a developmental coordination disorder and adults with limb-apraxia after stroke have deficits in visuomotor temporal integration [45, 47]. In addition, the degree of deficiency in visuomotor temporal integration correlates significantly with the severity of the movement disorder [45–47]. These previous studies showed that the impaired ability to compare self-generated movements and visual feedback to generate temporal errors leads to movement disorders.…”

“…Therefore, the current study investigated whether SR improved visuomotor temporal integration and/or hand motor function in healthy volunteers under a visuomotor temporal incongruent condition. The long-term objective of the present study is to examine the possibility of rehabilitation using SR for movement disorder patients with deficits in visuomotor temporal integration [45–47].…”