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Frequency-dependent oscillatory neural profiles during imitation

View Article: PubMed Central - PubMed

ABSTRACT

Imitation is a complex process that includes higher-order cognitive and motor function. This process requires an observation-execution matching system that transforms an observed action into an identical movement. Although the low-gamma band is thought to reflect higher cognitive processes, no studies have focused on it. Here, we used magnetoencephalography (MEG) to examine the neural oscillatory changes including the low-gamma band during imitation. Twelve healthy, right-handed participants performed a finger task consisting of four conditions (imitation, execution, observation, and rest). During the imitation and execution conditions, significant event-related desynchronizations (ERDs) were observed at the left frontal, central, and parietal MEG sensors in the alpha, beta, and low-gamma bands. Functional connectivity analysis at the sensor level revealed an imitation-related connectivity between a group of frontal sensors and a group of parietal sensors in the low-gamma band. Furthermore, source reconstruction with synthetic aperture magnetometry showed significant ERDs in the low-gamma band in the left sensorimotor area and the middle frontal gyrus (MFG) during the imitation condition when compared with the other three conditions. Our results suggest that the oscillatory neural activities of the low-gamma band at the sensorimotor area and MFG play an important role in the observation-execution matching system related to imitation.

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Related in: MedlinePlus

ERDs in the low-gamma band over the frontal areas at 300–500 ms after the presentation of Cue 2.ERDs were spatially averaged over voxels within each ROI. ERDs in the low-gamma band during imitation were significantly lower than those during the other three conditions at the left precentral gyrus and MFG (*p < 0.05, ANOVA and Tukey’s method). Low-gamma ERDs at the bilateral IFG differed significantly between the imitation and rest conditions but did not differ significantly between the imitation and execution conditions. Colors on the flattened cortical surface indicate each ROI. Error bars indicate standard error.
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f4: ERDs in the low-gamma band over the frontal areas at 300–500 ms after the presentation of Cue 2.ERDs were spatially averaged over voxels within each ROI. ERDs in the low-gamma band during imitation were significantly lower than those during the other three conditions at the left precentral gyrus and MFG (*p < 0.05, ANOVA and Tukey’s method). Low-gamma ERDs at the bilateral IFG differed significantly between the imitation and rest conditions but did not differ significantly between the imitation and execution conditions. Colors on the flattened cortical surface indicate each ROI. Error bars indicate standard error.

Mentions: In source space analysis, SAM was used to calculate the pseudo-t value for each condition, which is the contrast in source power between the baseline period and the period of interest normalized by sensor noise3637. Then, group statistical maps were generated to determine brain regions with significant oscillatory neural activity for each condition. The results showed that significant ERDs in the alpha and beta bands were similarly observed during the imitation and execution conditions at the left sensorimotor area (Figs 2 and S1) during the presentation of Cue 2, in which the participants watched an animated hand during the imitation condition and a static hand during the execution condition. Significant ERDs in the low-gamma band were observed at the left sensorimotor area just after Cue 2 during the imitation and execution conditions. However, these responses were maintained only during the imitation condition and spread to the left frontal gyri (Figs 2 and 3 and Table S1). Significant low-gamma ERDs were also observed in the right inferior/middle frontal gyri at 200–400 ms and 300–500 ms during the imitation and execution conditions (Figs 2, 3 and S1). Majority of these oscillatory changes peaked at 300–500 ms after presenting Cue 2 (Figs 2, 3, S1, S2, and S3) during each condition. Based on these results, ERDs for each frequency band were statistically compared among the conditions at 300–500 ms. The following six regions of interest (ROIs) were anatomically defined using the Montreal Neurological Institute (MNI) template: IFG, MFG, precentral gyrus, postcentral gyrus, inferior parietal lobule, and superior parietal lobule. The results showed that ERDs in the low-gamma band during the imitation condition were significantly lower than those during other conditions at the left precentral gyrus and MFG (F(3, 44) = 5.8, p = 0.002, one-way ANOVA) (Figs 4, S4 and S5). In addition, low-gamma ERDs at the bilateral IFG differed significantly between the imitation and rest conditions (left; F(3, 44) = 3.47, p = 0.024, right; F(3, 44) = 5.01, p = 0.0045, one-way ANOVA), whereas there were no significant differences between the imitation and execution conditions in these regions. Note that the colors on the flattened cortical surface in Fig. 4 indicate each ROI.


Frequency-dependent oscillatory neural profiles during imitation
ERDs in the low-gamma band over the frontal areas at 300–500 ms after the presentation of Cue 2.ERDs were spatially averaged over voxels within each ROI. ERDs in the low-gamma band during imitation were significantly lower than those during the other three conditions at the left precentral gyrus and MFG (*p < 0.05, ANOVA and Tukey’s method). Low-gamma ERDs at the bilateral IFG differed significantly between the imitation and rest conditions but did not differ significantly between the imitation and execution conditions. Colors on the flattened cortical surface indicate each ROI. Error bars indicate standard error.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5385530&req=5

f4: ERDs in the low-gamma band over the frontal areas at 300–500 ms after the presentation of Cue 2.ERDs were spatially averaged over voxels within each ROI. ERDs in the low-gamma band during imitation were significantly lower than those during the other three conditions at the left precentral gyrus and MFG (*p < 0.05, ANOVA and Tukey’s method). Low-gamma ERDs at the bilateral IFG differed significantly between the imitation and rest conditions but did not differ significantly between the imitation and execution conditions. Colors on the flattened cortical surface indicate each ROI. Error bars indicate standard error.
Mentions: In source space analysis, SAM was used to calculate the pseudo-t value for each condition, which is the contrast in source power between the baseline period and the period of interest normalized by sensor noise3637. Then, group statistical maps were generated to determine brain regions with significant oscillatory neural activity for each condition. The results showed that significant ERDs in the alpha and beta bands were similarly observed during the imitation and execution conditions at the left sensorimotor area (Figs 2 and S1) during the presentation of Cue 2, in which the participants watched an animated hand during the imitation condition and a static hand during the execution condition. Significant ERDs in the low-gamma band were observed at the left sensorimotor area just after Cue 2 during the imitation and execution conditions. However, these responses were maintained only during the imitation condition and spread to the left frontal gyri (Figs 2 and 3 and Table S1). Significant low-gamma ERDs were also observed in the right inferior/middle frontal gyri at 200–400 ms and 300–500 ms during the imitation and execution conditions (Figs 2, 3 and S1). Majority of these oscillatory changes peaked at 300–500 ms after presenting Cue 2 (Figs 2, 3, S1, S2, and S3) during each condition. Based on these results, ERDs for each frequency band were statistically compared among the conditions at 300–500 ms. The following six regions of interest (ROIs) were anatomically defined using the Montreal Neurological Institute (MNI) template: IFG, MFG, precentral gyrus, postcentral gyrus, inferior parietal lobule, and superior parietal lobule. The results showed that ERDs in the low-gamma band during the imitation condition were significantly lower than those during other conditions at the left precentral gyrus and MFG (F(3, 44) = 5.8, p = 0.002, one-way ANOVA) (Figs 4, S4 and S5). In addition, low-gamma ERDs at the bilateral IFG differed significantly between the imitation and rest conditions (left; F(3, 44) = 3.47, p = 0.024, right; F(3, 44) = 5.01, p = 0.0045, one-way ANOVA), whereas there were no significant differences between the imitation and execution conditions in these regions. Note that the colors on the flattened cortical surface in Fig. 4 indicate each ROI.

View Article: PubMed Central - PubMed

ABSTRACT

Imitation is a complex process that includes higher-order cognitive and motor function. This process requires an observation-execution matching system that transforms an observed action into an identical movement. Although the low-gamma band is thought to reflect higher cognitive processes, no studies have focused on it. Here, we used magnetoencephalography (MEG) to examine the neural oscillatory changes including the low-gamma band during imitation. Twelve healthy, right-handed participants performed a finger task consisting of four conditions (imitation, execution, observation, and rest). During the imitation and execution conditions, significant event-related desynchronizations (ERDs) were observed at the left frontal, central, and parietal MEG sensors in the alpha, beta, and low-gamma bands. Functional connectivity analysis at the sensor level revealed an imitation-related connectivity between a group of frontal sensors and a group of parietal sensors in the low-gamma band. Furthermore, source reconstruction with synthetic aperture magnetometry showed significant ERDs in the low-gamma band in the left sensorimotor area and the middle frontal gyrus (MFG) during the imitation condition when compared with the other three conditions. Our results suggest that the oscillatory neural activities of the low-gamma band at the sensorimotor area and MFG play an important role in the observation-execution matching system related to imitation.

No MeSH data available.


Related in: MedlinePlus