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Novel behavioral indicator of explicit awareness reveals temporal course of frontoparietal neural network facilitation during motor learning

View Article: PubMed Central - PubMed

ABSTRACT

Deficits in sequential motor learning have been observed in many patient populations. Having an understanding of the individual neural progression associated with sequential learning in healthy individuals may provide valuable insights for effective interventions with these patients. Due to individual variability in motor skill acquisition, the temporal course of such learning will be vary, suggesting a need for a more individualized approach. Knowing when a subject becomes aware of movement patterns may provide a marker with which to identify each individual’s learning time course. To avoid interfering with the incidental nature of discovery during learning, such an indicator requires an indirect, behaviorally-based approach. In Part I, our study aimed to identify a reliable behavioral indicator predictive of the presence of incidental explicit awareness in a sequential motor learning task. Part II, utilized the predictive indicator and EEG to provide neural validation of perceptual processing changes temporally correlated with the indicator. Results of Part I provide a reliable predictive indicator for the timing of explicit awareness development. Results from Part II demonstrates strong classification reliability, as well as a significant neural correlation with behavior for subjects developing awareness (EXP), not observed with subjects without awareness (NOEXP). Additionally, a temporal correlation of peak activation between neural regions was noted over frontoparietal regions, suggesting that the incidental discovery of motor patterns may involve a facilitative network during awareness development. The proposed indicator provides a tool in which to further examine potential impacts of awareness associated with incidental, or exploratory, motor learning, while the individual nature of the indicator provides a tool for monitoring progress in rehabilitative, exploratory motor learning paradigms.

No MeSH data available.


Related in: MedlinePlus

Neural activity for late N1 over parietal region.(a) Head maps for 9 periods of time during late N1 (140–170 msec). (b) ERP graph over parietal electrodes (P1, P2, P3, P4). (c) Dipole localization for late N1 component over left precuneus region. (d) ERP for left precuneus cluster. (e) Dipole localization for late N1 component over right precuneus region. (f) ERP for right precuneus cluster.
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pone.0175176.g005: Neural activity for late N1 over parietal region.(a) Head maps for 9 periods of time during late N1 (140–170 msec). (b) ERP graph over parietal electrodes (P1, P2, P3, P4). (c) Dipole localization for late N1 component over left precuneus region. (d) ERP for left precuneus cluster. (e) Dipole localization for late N1 component over right precuneus region. (f) ERP for right precuneus cluster.

Mentions: Fig 5a shows the head maps demonstrating activity changes over time, while Fig 5b shows ERP changes over the parietal lobe electrodes (P1, P3, P2, P4). Repeated measures ANOVA for TIMExAWARENESS demonstrated no main effect of time (F(8, 64) = 0.5811, p = 0.817), or awareness (F(1, 8) = 1.0328, p = 0.374), with an interaction effect nearing significance (F(8, 64) = 2.1245, p = 0.077). Post hoc analysis showed the EXP group had a significant difference in amplitude, relative to baseline, by Blocks 4–6, while the NOEXP group demonstrated a significant difference by Blocks 7–9. The NOEXP group maintained a relatively stable N1 for the remainder of the experiment, while the EXP group demonstrated a reduced N1 amplitude toward the end of the experiment, reaching levels similar to baseline by Blocks 19–21. ICA cluster analysis identified two clusters correlating with the late N1 component, with dipole localizations at the left and right precuneus (see Fig 5c and 5e for dipole centroid images and Table 4 for Talairach coordinates and cluster distribution). Cluster ERP’s revealed a larger late N1 for the EXP group over the left precuneus, while the NOEXP group demonstrated a larger late N1 component over the right precuneus (see Fig 5d and 5f). Based on the ERP differences noted between the left and right parietal dipole clusters, an additional repeated measures ANOVA for TIMExAWARENESS was made for the right (P2 & P4) and left (P1 & P3) parietal electrodes separately. The right parietal electrodes showed no main effect of time (F(8, 64) = 0.6419, p = 0.739), or awareness (F(1, 8) = 0.1.1044, p = 0.347) and no interaction effect (F(8, 64) = 1.5351, p = 0.206). The left parietal electrodes also showed no main effect of time (F(8, 64) = 0.6639, p = 0.769) or awareness (F(1, 8) = 0.9479, p = 0.404). However, there was an interaction effect seen (F(8, 64) = 2.7751, p = 0.024), with EXP subjects demonstrating a significant difference in amplitude, relative, to baseline, by Blocks 4–6, while the NOEXP group did not show a significant change in amplitude.


Novel behavioral indicator of explicit awareness reveals temporal course of frontoparietal neural network facilitation during motor learning
Neural activity for late N1 over parietal region.(a) Head maps for 9 periods of time during late N1 (140–170 msec). (b) ERP graph over parietal electrodes (P1, P2, P3, P4). (c) Dipole localization for late N1 component over left precuneus region. (d) ERP for left precuneus cluster. (e) Dipole localization for late N1 component over right precuneus region. (f) ERP for right precuneus cluster.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC5391991&req=5

pone.0175176.g005: Neural activity for late N1 over parietal region.(a) Head maps for 9 periods of time during late N1 (140–170 msec). (b) ERP graph over parietal electrodes (P1, P2, P3, P4). (c) Dipole localization for late N1 component over left precuneus region. (d) ERP for left precuneus cluster. (e) Dipole localization for late N1 component over right precuneus region. (f) ERP for right precuneus cluster.
Mentions: Fig 5a shows the head maps demonstrating activity changes over time, while Fig 5b shows ERP changes over the parietal lobe electrodes (P1, P3, P2, P4). Repeated measures ANOVA for TIMExAWARENESS demonstrated no main effect of time (F(8, 64) = 0.5811, p = 0.817), or awareness (F(1, 8) = 1.0328, p = 0.374), with an interaction effect nearing significance (F(8, 64) = 2.1245, p = 0.077). Post hoc analysis showed the EXP group had a significant difference in amplitude, relative to baseline, by Blocks 4–6, while the NOEXP group demonstrated a significant difference by Blocks 7–9. The NOEXP group maintained a relatively stable N1 for the remainder of the experiment, while the EXP group demonstrated a reduced N1 amplitude toward the end of the experiment, reaching levels similar to baseline by Blocks 19–21. ICA cluster analysis identified two clusters correlating with the late N1 component, with dipole localizations at the left and right precuneus (see Fig 5c and 5e for dipole centroid images and Table 4 for Talairach coordinates and cluster distribution). Cluster ERP’s revealed a larger late N1 for the EXP group over the left precuneus, while the NOEXP group demonstrated a larger late N1 component over the right precuneus (see Fig 5d and 5f). Based on the ERP differences noted between the left and right parietal dipole clusters, an additional repeated measures ANOVA for TIMExAWARENESS was made for the right (P2 & P4) and left (P1 & P3) parietal electrodes separately. The right parietal electrodes showed no main effect of time (F(8, 64) = 0.6419, p = 0.739), or awareness (F(1, 8) = 0.1.1044, p = 0.347) and no interaction effect (F(8, 64) = 1.5351, p = 0.206). The left parietal electrodes also showed no main effect of time (F(8, 64) = 0.6639, p = 0.769) or awareness (F(1, 8) = 0.9479, p = 0.404). However, there was an interaction effect seen (F(8, 64) = 2.7751, p = 0.024), with EXP subjects demonstrating a significant difference in amplitude, relative, to baseline, by Blocks 4–6, while the NOEXP group did not show a significant change in amplitude.

View Article: PubMed Central - PubMed

ABSTRACT

Deficits in sequential motor learning have been observed in many patient populations. Having an understanding of the individual neural progression associated with sequential learning in healthy individuals may provide valuable insights for effective interventions with these patients. Due to individual variability in motor skill acquisition, the temporal course of such learning will be vary, suggesting a need for a more individualized approach. Knowing when a subject becomes aware of movement patterns may provide a marker with which to identify each individual’s learning time course. To avoid interfering with the incidental nature of discovery during learning, such an indicator requires an indirect, behaviorally-based approach. In Part I, our study aimed to identify a reliable behavioral indicator predictive of the presence of incidental explicit awareness in a sequential motor learning task. Part II, utilized the predictive indicator and EEG to provide neural validation of perceptual processing changes temporally correlated with the indicator. Results of Part I provide a reliable predictive indicator for the timing of explicit awareness development. Results from Part II demonstrates strong classification reliability, as well as a significant neural correlation with behavior for subjects developing awareness (EXP), not observed with subjects without awareness (NOEXP). Additionally, a temporal correlation of peak activation between neural regions was noted over frontoparietal regions, suggesting that the incidental discovery of motor patterns may involve a facilitative network during awareness development. The proposed indicator provides a tool in which to further examine potential impacts of awareness associated with incidental, or exploratory, motor learning, while the individual nature of the indicator provides a tool for monitoring progress in rehabilitative, exploratory motor learning paradigms.

No MeSH data available.


Related in: MedlinePlus