Neural Mechanism of Altered Limb Perceptions Caused by Temporal Sensorimotor Incongruence

Abstract

Previous studies have demonstrated that patients with strokes or pathological pain suffer distorted limb ownership and an inability to perceive their affected limbs as a part of their bodies. These disturbances are apparent in experiments showing time delays between motor commands and visual feedback. The experimental paradigm manipulating temporal delay is considered possible to clarify, in detail, the degree of altered limb perception, peculiarity and movement disorders that are caused by temporal sensorimotor incongruence. However, the neural mechanisms of these body perceptions, peculiarity and motor control remain unknown. In this experiment, we used exact low-resolution brain electromagnetic tomography (eLORETA) with independent component analysis (ICA) to clarify the neural mechanisms of altered limb perceptions caused by temporal sensorimotor incongruence. Seventeen healthy participants were recruited, and temporal sensorimotor incongruence was systematically evoked using a visual feedback delay system. Participants periodically extended their right wrists while viewing video images of their hands that were delayed by 0, 150, 250, 350 and 600 ms. To investigate neural mechanisms, altered limb perceptions were then rated using the 7-point Likert scale and brain activities were concomitantly examined with electroencephalographic (EEG) analyses using eLORETA-ICA. These experiments revealed that peculiarities are caused prior to perceptions of limb loss and heaviness. Moreover, we show that supplementary motor and parietal association areas are involved in changes of peculiarity, limb loss, heaviness and movement accuracy due to temporal sensorimotor incongruence. We suggest that abnormalities in these areas contribute to neural mechanisms that modify altered limb perceptions and movement accuracy.

Keywords: altered limb perceptions; eLORETA-ICA; electroencephalogram; exact low-resolution brain electromagnetic tomography (eLORETA); parietal association area; peculiarity; supplementary motor area; temporal sensorimotor incongruence.

Figure 1

Demonstration of the experimental setup. Participants watched an image of their moving right hand that was delayed following their actual movement. The conditions of the visual feedback delay were 0, 150, 250, 350 and 600 ms delay conditions.

Figure 2

Degree of subjective and kinematic data detected under the five conditions. Boxes (median [interquartile range]) represent 7-point Likert scale scores for peculiarity (A), heaviness (B), lost limb (C) and median of mean absolute deviation (MAD; D). *Significant change (Wilcoxon test with Bonferroni correction to examine the differences among the five conditions P < 0.012, p-value adjusted for multiple comparisons).

Figure 3

Correlation between subjective data and kinematic data for the 250, 350 and 600 ms delay condition. (A) Scatter plot showing a significant negative correlation between the heaviness and the MAD in 250 ms delay condition. (B) Scatter plot showing a significant negative correlation between the heaviness and the MAD in 350 ms delay condition. (C) Scatter plot showing a significant negative correlation between the heaviness and the MAD in 600 ms delay condition.

Figure 4

Correlation between 150 ms delay condition components and subjective data. (A) Component 2 corresponds to the ventromedial prefrontal cortex (vmPFC) in Theta, Alpha1 and Beta2 frequency band. The red colors indicate increased activity under the 150 ms delay condition. (B) Scatter plot showing a significant positive correlation between the peculiarity and the Beta2/theta ratio in Rt. vmPFC (x = 5, y = 65, z = −15). (C) Scatter plot showing a significant positive correlation between the peculiarity and the Beta2/alpha1 ratio in Rt. vmPFC (x = 5, y = 65, z = −15). (D) Scatter plot showing a significant positive correlation between the peculiarity and the Beta2/alpha1 ratio in Lt. vmPFC (x = −5, y = 60, z = −20).

Figure 5

Correlation between 600 ms delay condition components and subjective data. (A) Component 1 corresponds to the dorsolateral PFC (DLPFC), supplementary motor area (SMA) and superior parietal lobule (SPL) in Gamma frequency band. The red colors indicate increased activity under the 600 ms delay condition. The blue colors indicate decreased activity under the 600 ms delay condition. (B) Scatter plot showing a significant positive correlation between the peculiarity and the Lt. SMA/Rt. DLPFC ratio in gamma band. (C) Scatter plot showing a significant positive correlation between the peculiarity and the Rt. SPL/Rt. DLPFC ratio in gamma band. (D) Scatter plot showing a significant negative correlation between the heaviness and the Theta/gamma ratio in Lt. SMA (x = −5, y = −10, z = 65). Rt. DLPFC (x = 45, y = 40, z = 30), Rt. SPL (x = 35, y = −55, z = 60).

Figure 6

Correlation between 600 ms delay condition component and kinematic data. (A) Component 10 corresponds to the inferior parietal lobule (IPL) in Beta3 and Gamma frequency band. The red colors indicate increased activity under the 600 ms delay condition. (B) Scatter plot showing a significant negative correlation between the mean of MAD and the Beta3/gamma ratio in Rt. IPL (x = 65, y = −45, z = 25).

Figure 7

Correlation between 600 ms delay condition component and subjective data. (A) Component 16 corresponds to the SMA in Alpha1 and Beta3 frequency band. The blue colors indicate decreased activity under the 600 ms delay condition. (B) Scatter plot showing a significant positive correlation between the lost limb and the Alpha1/beta3 ratio in Lt. SMA (x = −5, y = −10, z = 65).