Functional Connectivity Between Motor and Mid-Frontal Areas During Vicarious Reward Revealed via EEG Time-Frequency Analysis.

Vicarious reward is a phenomenon in which an individual feels as if he/she has received a reward as the result of watching someone else receive a reward. In this study, we used electroencephalography to investigate brain activity while participants watched a preferred player win a competitive game (Rock-Paper-Scissors game). In the experimental task, movie clips showed right hand of the two players and played Rock-Paper-Scissors game. We asked participants to explicitly support or "cheer" for a specific player, and then examined brain activity associated with vicarious reward. For the observed hand movement, previous findings showed that the event-related desynchronization of mu band (8-14 Hz) appeared at the contra-lateral central electrode to the observed hand (If someone sees the right-hand movement, the left central electrode shows the event-related desynchronization of mu-band). During observation of the player, we detected event-related desynchronization of mu band activity in the contra-lateral central electrode as well as mid-frontal beta band (15-22 Hz) activation when the preferred player won. Furthermore, functional connectivity analysis revealed a strong phase synchronization between the contra-lateral central electrode and mid-frontal electrode in the mu band when participants received the vicarious reward. Cross-frequency coupling analysis revealed functional integration between the mu and beta bands at mid-frontal electrode. These results indicate the interaction of mu band observed at contra-lateral electrode and beta band observed at mid-frontal electrode coupling, suggesting a link between the mirror neuron system and the reward system during vicarious reward.

Sensorimotor and Posterior Brain Activations During the Observation of Illusory Embodied Fake Hand Movement.

In the rubber hand illusion (RHI), the subject recognizes a fake hand as his or her own. We recently found that the observation of embodied fake hand movement elicited mu-rhythm (8-13 Hz) desynchronization on electroencephalography (EEG), suggesting brain activation in the sensorimotor regions. However, it is known that mu-rhythm desynchronization during action observation is confounded with occipital alpha-rhythm desynchronization, which is modulated by attention. This study examined the independence of brain activities in the sensorimotor and occipital regions relating to the movement observation under the RHI. The invisible participant's left and fake right hands were stroked simultaneously, which was interrupted by unexpected fake hand movements. A mirror-reversed image of the fake hand was shown on a monitor in front of the participant with a delay of 80, 280, or 480 ms. Illusion strength decreased as a function of the delay. EEG independent component analysis (ICA) and ICA clustering revealed six clusters with observation-induced desynchronization of 8-13 Hz frequency band. In the right sensorimotor cluster, mu-rhythm desynchronization was the greatest under the 80-ms delay, while alpha-rhythm desynchronization of the occipital clusters did not show delay-dependence. These results suggest that brain activation in the sensorimotor areas (i.e., mu-rhythm desynchronization) induced by embodied fake hand movement is independent of that in the occipital areas (alpha-rhythm desynchronization).

Simultaneous EEG-NIRS Measurement of the Inferior Parietal Lobule During a Reaching Task With Delayed Visual Feedback.

We investigated whether the inferior parietal lobule (IPL) responds in real-time to multisensory inconsistency during movement. The IPL is thought to be involved in both the detection of inconsistencies in multisensory information obtained during movement and that obtained during self-other discrimination. However, because of the limited temporal resolution of conventional neuroimaging techniques, it is difficult to distinguish IPL activity during movement from that during self-other discrimination. We simultaneously conducted electroencephalography (EEG) and near-infrared spectroscopy (NIRS) with the goal of examining IPL activity with a high spatiotemporal resolution during single reaching movements. Under a visual feedback-delay condition, gamma event-related synchronization (γ-ERS), i.e., an increase in gamma (31-47 Hz) EEG power occurred during reaching movements. This γ-ERS is considered to reflect processing of information about prediction errors. To integrate this temporal information with spatial information from the NIRS signals, we developed a new analysis technique that enabled estimation of the regions that show a hemodynamic response characterized by EEG fluctuation present in the visual feedback-delay condition. As a result, IPL activity was explained by γ-ERS specific to visual feedback delay during movements. Thus, we succeeded in demonstrating real-time activation of the IPL in response to multisensory inconsistency. However, we did not find any correlation between either IPL activity or γ-ERS with the sense of agency. Therefore, our results suggest that while the IPL is influenced by prediction error signals, it does not engage in direct processing underlying the conscious experience of making a movement, which is the foundation of self-other discrimination.

The relationship and difference between delay detection ability and judgment of sense of agency.

Judgment of agency involves the comparison of motor intention and proprioceptive/visual feedback, in addition to a range of cognitive factors. However, few studies have experimentally examined the differences or correlations between delay detection ability and judgment of agency. Thus, the present study investigated the relationship between delay detection ability and agency judgment using the delay detection task and the agency attribution task. Fifty-eight participants performed the delay detection and agency attribution tasks, and the time windows of each measure were analyzed using logistic curve fitting. The results revealed that the time window of judgment of agency was significantly longer than that of delay detection, and there was a slight correlation between the time windows in each task. The results supported a two-step model of agency, suggesting that judgment of agency involved not only comparison of multisensory information but also several cognitive factors. The study firstly revealed the model in psychophysical experiments.

Stochastic resonance improves visuomotor temporal integration in healthy young adults.

Mechanical and electrical noise stimulation to the body is known to improve the sensorimotor system. This improvement is related to stochastic resonance (SR), a phenomenon described as a "noise benefit" to various sensory and motor systems. The current study investigated the influence of SR on visuomotor temporal integration and hand motor function under delayed visual feedback in healthy young adults. The purpose of this study was to measure the usefulness of SR as a neurorehabilitation device for disorders of visuomotor temporal integration. Thirty healthy volunteers underwent detection tasks and hand motor function tests under delayed visual feedback, with or without SR. Of the 30 participants, 15 carried out the tasks under delayed visual feedback in the order of SR on-condition, off-condition, off-condition, and on-condition. The remaining 15 participants conducted the experimental tasks in the order of SR off-condition, on-condition, on-condition, and off-condition. Comparisons of the delay detection threshold (DDT), steepness of the delay detection probability curves, box and block test (BBT) scores, and nine-hole peg test (NHPT) scores between the SR on- and off-conditions were performed. The DDT under the SR on-condition was significantly shortened compared with the SR off-condition. There was no significant difference between the SR on- and off-conditions for the steepness of the delay detection probability curves, BBT scores, and NHPT scores. SR improved visuomotor temporal integration in healthy young adults, and may therefore improve movement disorders in patients with impaired visuomotor temporal integration. However, because the current results showed that SR did not improve hand motor function under delayed visual feedback, it may not improve motor function when a large distortion of visuomotor temporal integration is present. Further studies are required considering several limitations of the current study, and future clinical trials are necessary to verify the effects of motor training using SR for the treatment of visuomotor temporal integration disorders.

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

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.

Manual Dexterity Is a Strong Predictor of Visuo-Motor Temporal Integration in Children.

Although visuo-motor temporal integration in children is suggested to be related to motor control and motor learning, its relevance is still unclear. On the other hand, visuo-motor temporal integration ability undergoes developmental changes with age. In the current correlational study, we measured manual dexterity and visuo-motor temporal integration ability in 132 children with typical development (age, 4-15 years) and investigated the relationship between the two functions. The Movement Assessment Battery for Children-2nd edition was used as an indicator of manual dexterity. The delay detection threshold (DDT) and steepness of the probability curve for delay detection, which was measured by the delayed visual feedback detection task for self-generated movement, were used as indices of the visuo-motor temporal integration ability. The results indicated significant correlations between manual dexterity/age and DDT/steepness of the probability curve for delay detection. In addition, hierarchical multiple regression analysis showed that both manual dexterity and age significantly contributed to visuo-motor temporal integration, indicating a better fit than when only age was employed as an independent variable. Importantly, there was no interaction effect between age and manual dexterity. These findings were the first to suggest that manual dexterity is a significant predictor of visuo-motor temporal integration ability in children, regardless of age. The present study validated the important relationship between visuo-motor temporal integration and manual dexterity in children. Considering the limitations of the current study, including the non-homogeneous sample, further studies are still warranted to validate the results.

Deficits in Visuo-Motor Temporal Integration Impacts Manual Dexterity in Probable Developmental Coordination Disorder.

The neurological basis of developmental coordination disorder (DCD) is thought to be deficits in the internal model and mirror-neuron system (MNS) in the parietal lobe and cerebellum. However, it is not clear if the visuo-motor temporal integration in the internal model and automatic-imitation function in the MNS differs between children with DCD and those with typical development (TD). The current study aimed to investigate these differences. Using the manual dexterity test of the Movement Assessment Battery for Children (second edition), the participants were either assigned to the probable DCD (pDCD) group or TD group. The former was comprised of 29 children with clumsy manual dexterity, while the latter consisted of 42 children with normal manual dexterity. Visuo-motor temporal integration ability and automatic-imitation function were measured using the delayed visual feedback detection task and motor interference task, respectively. Further, the current study investigated whether autism-spectrum disorder (ASD) traits, attention-deficit hyperactivity disorder (ADHD) traits, and depressive symptoms differed among the two groups, since these symptoms are frequent comorbidities of DCD. In addition, correlation and multiple regression analyses were performed to extract factors affecting clumsy manual dexterity. In the results, the delay-detection threshold (DDT) and steepness of the delay-detection probability curve, which indicated visuo-motor temporal integration ability, were significantly prolonged and decreased, respectively, in children with pDCD. The interference effect, which indicated automatic-imitation function, was also significantly reduced in this group. These results highlighted that children with clumsy manual dexterity have deficits in visuo-motor temporal integration and automatic-imitation function. There was a significant correlation between manual dexterity, and measures of visuo-motor temporal integration, and ASD traits and ADHD traits and ASD. Multiple regression analysis revealed that the DDT, which indicated visuo-motor temporal integration, was the greatest predictor of poor manual dexterity. The current results supported and provided further evidence for the internal model deficit hypothesis. Further, they suggested a neurorehabilitation technique that improved visuo-motor temporal integration could be therapeutically effective for children with DCD.

Spontaneous imitative movements induced by an illusory embodied fake hand.

In the rubber hand illusion (RHI), individuals perceive a fake hand as their own when the hidden real hand and visible fake hand are synchronously stroked. Several RHI studies have reported that visual manipulation of the embodied fake hand inversely affects the perceptual processing of the observer's own hand (e.g., thermal or pain sensitivity). In this study, we examined whether motor manipulation of the fake hand similarly affects the observer's motor system. Our study employed a novel RHI paradigm wherein stroking was interrupted by unexpected movement of the fake hand (i.e., finger spreading) while measuring electroencephalography (EEG). We found that participants often spontaneously moved their hands in accordance with the movement of the fake hand only in the RHI (synchronous) sessions. EEG analyses revealed enhanced neural activation (mu-rhythm desynchronization) of the motor system during observation of the fake hand movement. Moreover, motor activation was greater in the synchronous than in the asynchronous condition and significantly correlated with the feeling of body ownership over the fake hand. These findings provide strong behavioral and neurophysiological evidence of 'motor back projection', in which the movement of an illusory embodied body part is inversely transferred to the sensorimotor system of the observer.

Sensorimotor incongruence alters limb perception and movement.

Altered limb ownership or heaviness has been observed in patients with hemiplegia, chronic pain, and several other conditions. Although these sensations are thought to be caused by sensorimotor incongruence, few studies have systematically verified this relationship. In addition, it remains unclear whether these subjective sensations affect movement execution. In a psychophysical experiment, we systematically investigated the relationships between sensorimotor integration and subjective limb perception, such as sense of ownership/heaviness, and verified the relationship between subjective limb perception and movement execution. Thirty-nine healthy participants were enrolled, and a visual feedback delay system was used to systematically evoke sensorimotor incongruence. Participants periodically flexed and extended their wrist while seeing a delayed image of their hand under five delay conditions (0, 150, 250, 350, 600ms). During wrist movement, electromyography (EMG) activity in flexor carpi radialis (FCR) was recorded. Also, to analyze the change in muscle activity and movement speed, the values of integral and peak frequency were calculated. To record changes in the subjective limb perception of the altered limb ownership and heaviness, we used a 7-point Likert scale for each participant. We found that altered ownership and heaviness increased with increasing feedback delay. Also, muscle activity and movement speed decreased with visual feedback delay. There was no significant correlation between subjective altered limb perception (i.e., altered limb ownership and heaviness) and muscle activity or movement speed. We systematically demonstrated that limb ownership, heaviness, muscle activation and movement speed were altered by sensorimotor incongruence. However, our study did not reveal the relationships between these factors. These results indicate the existence of different mechanisms governing subjective limb perception and movement execution. In the future, we should consider rehabilitation methods to improve sensorimotor incongruence.

Simultaneous measurement of electroencephalography and near-infrared spectroscopy during voluntary motor preparation.

We investigated the relationship between electrophysiological activity and haemodynamic response during motor preparation by simultaneous recording of electroencephalography (EEG) and near-infrared spectroscopy (NIRS). It is still unknown how exactly EEG signals correlate with the haemodynamic response, although the activation in the premotor area during motor preparation has been captured by EEG and haemodynamic approaches separately. We conducted EEG-NIRS simultaneous recordings over the sensorimotor area with a self-paced button press task. Participants were instructed to press a button at their own pace after a cue was shown. The result showed that the readiness potential (RP), a negative slow potential shift occurring during motor preparation, on C3 in the extended 10-20 system occurred about 1000 ms before the movement onset. An increase in concentration of oxyhaemoglobin (oxyHb) in the premotor cortex during motor preparation was also confirmed by NIRS, which resulted in a significant correlation between the amplitude of the RP and the change in oxyHb concentration (Pearson's correlation r(2) = 0.235, p = 0.03). We show that EEG-NIRS simultaneous recording can demonstrate the correlation between the RP and haemodynamic response in the premotor cortex contralateral to the performing hand.