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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.

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Neural activity for P2 over left frontocentral region.(a) Head maps for 9 periods of time during P2 (180–210 msec). (b) ERP graph over left frontocentral electrodes (C1A, CZA, C1, CZ). (c) Dipole localization for P2 component over left supplementary motor area.
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pone.0175176.g006: Neural activity for P2 over left frontocentral region.(a) Head maps for 9 periods of time during P2 (180–210 msec). (b) ERP graph over left frontocentral electrodes (C1A, CZA, C1, CZ). (c) Dipole localization for P2 component over left supplementary motor area.

Mentions: Fig 6a shows head map changes for the P2 time period demonstrating the peak activity at Blocks 13–15 and 22–24. The P2 ERP component (see Fig 6b) showed no significant main effect of time (F(8, 64) = 1.1908, p = 0.392) or awareness (F(1, 8) = 1.6912, p = 0.247), but did reveal a significant interaction effect (F(8, 64) = 3.7882, p = 0.002). Post hoc analysis revealed the EXP group had a significant difference in peak amplitude, relative to baseline compared to the NOEXP group. The largest significant differences were noted to occur at Blocks 13–15 and Blocks 22–24, again clustering in two time periods similar to the Early and Late Learner behaviors. The NOEXP group did not demonstrate a significant change from baseline over the course of the experiment. The ICA cluster correlating with the P2 component showed a dipole localization at the left supplementary motor area (SMA) as shown in Fig 6c (refer also to Table 4 for Talairach coordinates and cluster distribution).


Novel behavioral indicator of explicit awareness reveals temporal course of frontoparietal neural network facilitation during motor learning
Neural activity for P2 over left frontocentral region.(a) Head maps for 9 periods of time during P2 (180–210 msec). (b) ERP graph over left frontocentral electrodes (C1A, CZA, C1, CZ). (c) Dipole localization for P2 component over left supplementary motor area.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5391991&req=5

pone.0175176.g006: Neural activity for P2 over left frontocentral region.(a) Head maps for 9 periods of time during P2 (180–210 msec). (b) ERP graph over left frontocentral electrodes (C1A, CZA, C1, CZ). (c) Dipole localization for P2 component over left supplementary motor area.
Mentions: Fig 6a shows head map changes for the P2 time period demonstrating the peak activity at Blocks 13–15 and 22–24. The P2 ERP component (see Fig 6b) showed no significant main effect of time (F(8, 64) = 1.1908, p = 0.392) or awareness (F(1, 8) = 1.6912, p = 0.247), but did reveal a significant interaction effect (F(8, 64) = 3.7882, p = 0.002). Post hoc analysis revealed the EXP group had a significant difference in peak amplitude, relative to baseline compared to the NOEXP group. The largest significant differences were noted to occur at Blocks 13–15 and Blocks 22–24, again clustering in two time periods similar to the Early and Late Learner behaviors. The NOEXP group did not demonstrate a significant change from baseline over the course of the experiment. The ICA cluster correlating with the P2 component showed a dipole localization at the left supplementary motor area (SMA) as shown in Fig 6c (refer also to Table 4 for Talairach coordinates and cluster distribution).

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