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A subcortical oscillatory network contributes to recovery of hand dexterity after spinal cord injury.

Nishimura Y, Morichika Y, Isa T - Brain (2009)

Bottom Line: Activities of antagonist muscle pairs showed co-activation and oscillated coherently at frequencies of 30-46 Hz (gamma-band) by 1-month post-lesion.Such gamma-band inter-muscular coupling was not observed pre-lesion, but emerged and was strengthened and distributed over a wide range of hand/arm muscles along with the recovery.Neither the beta-band (14-30 Hz) cortico-muscular coupling observed pre-lesion nor a gamma-band oscillation was observed in the motor cortex post-lesion.

View Article: PubMed Central - PubMed

Affiliation: Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan. yukio@u.washington.edu

ABSTRACT
Recent studies have shown that after partial spinal-cord lesion at the mid-cervical segment, the remaining pathways compensate for restoring finger dexterity; however, how they control hand/arm muscles has remained unclear. To elucidate the changes in dynamic properties of neural circuits connecting the motor cortex and hand/arm muscles, we investigated the cortico- and inter-muscular couplings of activities throughout the recovery period after the spinal-cord lesion. Activities of antagonist muscle pairs showed co-activation and oscillated coherently at frequencies of 30-46 Hz (gamma-band) by 1-month post-lesion. Such gamma-band inter-muscular coupling was not observed pre-lesion, but emerged and was strengthened and distributed over a wide range of hand/arm muscles along with the recovery. Neither the beta-band (14-30 Hz) cortico-muscular coupling observed pre-lesion nor a gamma-band oscillation was observed in the motor cortex post-lesion. We propose that a subcortical oscillator commonly recruits hand/arm muscles, via remaining pathways such as reticulospinal and/or propriospinal tracts, independent of cortical oscillation, and contributes to functional recovery.

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Long-term synchronization of muscles (BB, FCR, ED23 and ADP) recorded at various times before and after the l-CST lesion. Data were obtained from 0.5 s before the increase of force in the thumb to the end of force production. (A–D) From preoperatively (A), postoperative day 14 (B), postoperative day 34 (C) and postoperative day 92 (D). (a) the EMG activity from BB (top), FCR (second row), ED23 (third row), ADP (forth row) and force trajectory of thumb (bottom row). (b) Cross-correlograms between ED23 and ADP. The grey vertical lines represent zero-lag time in the cross-correlograms. These data were obtained from Monkey Be. (E and F) Changes in long-term synchronization of muscle pairs during recovery in Monkey Be (E) and Monkey Mu (F). Correlation coefficients of the activities of muscle pairs at zero-lag time, indicated with vertical grey lines in each cross-correlograms, are plotted. (a) Correlations between ED23 activity and that of a variety of other muscles (see inset). (b) Correlations between ADP activity and that of a variety of other muscles (see inset).
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Figure 4: Long-term synchronization of muscles (BB, FCR, ED23 and ADP) recorded at various times before and after the l-CST lesion. Data were obtained from 0.5 s before the increase of force in the thumb to the end of force production. (A–D) From preoperatively (A), postoperative day 14 (B), postoperative day 34 (C) and postoperative day 92 (D). (a) the EMG activity from BB (top), FCR (second row), ED23 (third row), ADP (forth row) and force trajectory of thumb (bottom row). (b) Cross-correlograms between ED23 and ADP. The grey vertical lines represent zero-lag time in the cross-correlograms. These data were obtained from Monkey Be. (E and F) Changes in long-term synchronization of muscle pairs during recovery in Monkey Be (E) and Monkey Mu (F). Correlation coefficients of the activities of muscle pairs at zero-lag time, indicated with vertical grey lines in each cross-correlograms, are plotted. (a) Correlations between ED23 activity and that of a variety of other muscles (see inset). (b) Correlations between ADP activity and that of a variety of other muscles (see inset).

Mentions: For coherence and cross-correlation analyses of LFP and EMG signals, a Spike2 software script was used. Coherence and cross-correlation estimates for CMC and IMC (Figs 3 and 5) were calculated during the hold phase of force production. Coherence and power spectra were calculated by averaging across segments, using non-overlapping segments composed of 2048 sample points. CMC or IMC was considered significant when it was >95% confidence limits computed from the number of epochs as described elsewhere (Halliday et al., 1995). As 240 epoch data were used for calculating coherence in this study, 95% confidence limit was 0.0125, which was indicated with a grey horizontal line in each coherence plot. The penetration track with the highest CMC was selected for further analyses. Cross-correlation estimates of long-term synchronization in Fig. 4 were calculated from 0.5 s before the increase of thumb force to the end of force production. We excluded records from muscle pairs demonstrating cross-talk between the EMG records as evidenced by high, narrow peaks in the cross-correlogram at the zero-lag time and a high degree of coherence at all frequencies. In Monkey Be, the cross-talk was detected from a muscle pair, ADP-FDI in all the recording sessions. In Monkey Mu, the cross-talk was detected from muscle pair ADP-FDI during all the recording sessions, ED23-FCU, ED23-BB, ADP-FCU on postoperative day 9, ED23-FCU, ED23-BB, ADP-FDS and ADP-BB on postoperative day 13. These data were not used for further analysis.


A subcortical oscillatory network contributes to recovery of hand dexterity after spinal cord injury.

Nishimura Y, Morichika Y, Isa T - Brain (2009)

Long-term synchronization of muscles (BB, FCR, ED23 and ADP) recorded at various times before and after the l-CST lesion. Data were obtained from 0.5 s before the increase of force in the thumb to the end of force production. (A–D) From preoperatively (A), postoperative day 14 (B), postoperative day 34 (C) and postoperative day 92 (D). (a) the EMG activity from BB (top), FCR (second row), ED23 (third row), ADP (forth row) and force trajectory of thumb (bottom row). (b) Cross-correlograms between ED23 and ADP. The grey vertical lines represent zero-lag time in the cross-correlograms. These data were obtained from Monkey Be. (E and F) Changes in long-term synchronization of muscle pairs during recovery in Monkey Be (E) and Monkey Mu (F). Correlation coefficients of the activities of muscle pairs at zero-lag time, indicated with vertical grey lines in each cross-correlograms, are plotted. (a) Correlations between ED23 activity and that of a variety of other muscles (see inset). (b) Correlations between ADP activity and that of a variety of other muscles (see inset).
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Related In: Results  -  Collection

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Figure 4: Long-term synchronization of muscles (BB, FCR, ED23 and ADP) recorded at various times before and after the l-CST lesion. Data were obtained from 0.5 s before the increase of force in the thumb to the end of force production. (A–D) From preoperatively (A), postoperative day 14 (B), postoperative day 34 (C) and postoperative day 92 (D). (a) the EMG activity from BB (top), FCR (second row), ED23 (third row), ADP (forth row) and force trajectory of thumb (bottom row). (b) Cross-correlograms between ED23 and ADP. The grey vertical lines represent zero-lag time in the cross-correlograms. These data were obtained from Monkey Be. (E and F) Changes in long-term synchronization of muscle pairs during recovery in Monkey Be (E) and Monkey Mu (F). Correlation coefficients of the activities of muscle pairs at zero-lag time, indicated with vertical grey lines in each cross-correlograms, are plotted. (a) Correlations between ED23 activity and that of a variety of other muscles (see inset). (b) Correlations between ADP activity and that of a variety of other muscles (see inset).
Mentions: For coherence and cross-correlation analyses of LFP and EMG signals, a Spike2 software script was used. Coherence and cross-correlation estimates for CMC and IMC (Figs 3 and 5) were calculated during the hold phase of force production. Coherence and power spectra were calculated by averaging across segments, using non-overlapping segments composed of 2048 sample points. CMC or IMC was considered significant when it was >95% confidence limits computed from the number of epochs as described elsewhere (Halliday et al., 1995). As 240 epoch data were used for calculating coherence in this study, 95% confidence limit was 0.0125, which was indicated with a grey horizontal line in each coherence plot. The penetration track with the highest CMC was selected for further analyses. Cross-correlation estimates of long-term synchronization in Fig. 4 were calculated from 0.5 s before the increase of thumb force to the end of force production. We excluded records from muscle pairs demonstrating cross-talk between the EMG records as evidenced by high, narrow peaks in the cross-correlogram at the zero-lag time and a high degree of coherence at all frequencies. In Monkey Be, the cross-talk was detected from a muscle pair, ADP-FDI in all the recording sessions. In Monkey Mu, the cross-talk was detected from muscle pair ADP-FDI during all the recording sessions, ED23-FCU, ED23-BB, ADP-FCU on postoperative day 9, ED23-FCU, ED23-BB, ADP-FDS and ADP-BB on postoperative day 13. These data were not used for further analysis.

Bottom Line: Activities of antagonist muscle pairs showed co-activation and oscillated coherently at frequencies of 30-46 Hz (gamma-band) by 1-month post-lesion.Such gamma-band inter-muscular coupling was not observed pre-lesion, but emerged and was strengthened and distributed over a wide range of hand/arm muscles along with the recovery.Neither the beta-band (14-30 Hz) cortico-muscular coupling observed pre-lesion nor a gamma-band oscillation was observed in the motor cortex post-lesion.

View Article: PubMed Central - PubMed

Affiliation: Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan. yukio@u.washington.edu

ABSTRACT
Recent studies have shown that after partial spinal-cord lesion at the mid-cervical segment, the remaining pathways compensate for restoring finger dexterity; however, how they control hand/arm muscles has remained unclear. To elucidate the changes in dynamic properties of neural circuits connecting the motor cortex and hand/arm muscles, we investigated the cortico- and inter-muscular couplings of activities throughout the recovery period after the spinal-cord lesion. Activities of antagonist muscle pairs showed co-activation and oscillated coherently at frequencies of 30-46 Hz (gamma-band) by 1-month post-lesion. Such gamma-band inter-muscular coupling was not observed pre-lesion, but emerged and was strengthened and distributed over a wide range of hand/arm muscles along with the recovery. Neither the beta-band (14-30 Hz) cortico-muscular coupling observed pre-lesion nor a gamma-band oscillation was observed in the motor cortex post-lesion. We propose that a subcortical oscillator commonly recruits hand/arm muscles, via remaining pathways such as reticulospinal and/or propriospinal tracts, independent of cortical oscillation, and contributes to functional recovery.

Show MeSH
Related in: MedlinePlus