Limits...
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.

Show MeSH

Related in: MedlinePlus

Oscillatory coupling of muscle pair (ED23 and ADP) activities recorded at various times before and after the l-CST lesion. (A–D) preoperatively (A), postoperative day 14 (B), postoperative day 34 (C) and postoperative day 92 (D). (a) The rectified EMG activity from ED23 (top) and ADP (bottom). Data obtained during the hold phase of precision grip in Monkey Be. (b and c) power spectra of ED23 and ADP, respectively. (d) Coherence between ED23 and ADP. In the coherence plots, the grey horizontal lines represent the 95% confidence limit (0.0125). (e) Cross-correlograms between ED23 and ADP. In cross-correlograms, the y-axes on the right and left sides indicate the absolute and relative values, respectively. The grey vertical lines in the cross-correlograms represent the zero-lag time. (E and F) Changes in the 30–46-Hz IMC during recovery in Monkey Be (E) and Monkey Mu (F). (a) Coupling between ED23 and a variety of other muscles (see inset). (b) Coupling between ADP and a variety of other muscles (see inset). n.s. in (a) and (b) indicates coherence values that were not significant. The grey horizontal lines in (a) and (b) represent the 95% confidence limit of coherence.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2664448&req=5

Figure 5: Oscillatory coupling of muscle pair (ED23 and ADP) activities recorded at various times before and after the l-CST lesion. (A–D) preoperatively (A), postoperative day 14 (B), postoperative day 34 (C) and postoperative day 92 (D). (a) The rectified EMG activity from ED23 (top) and ADP (bottom). Data obtained during the hold phase of precision grip in Monkey Be. (b and c) power spectra of ED23 and ADP, respectively. (d) Coherence between ED23 and ADP. In the coherence plots, the grey horizontal lines represent the 95% confidence limit (0.0125). (e) Cross-correlograms between ED23 and ADP. In cross-correlograms, the y-axes on the right and left sides indicate the absolute and relative values, respectively. The grey vertical lines in the cross-correlograms represent the zero-lag time. (E and F) Changes in the 30–46-Hz IMC during recovery in Monkey Be (E) and Monkey Mu (F). (a) Coupling between ED23 and a variety of other muscles (see inset). (b) Coupling between ADP and a variety of other muscles (see inset). n.s. in (a) and (b) indicates coherence values that were not significant. The grey horizontal lines in (a) and (b) represent the 95% confidence limit of coherence.

Mentions: In addition to the postoperative emergence of long-term synchrony, the EMG activities of muscles ADP and ED23 also became oscillatory and coherent. Prior to spinal cord lesions, the EMG activity of the ED23 muscle contained frequency components over a broad range (Fig. 5Ab) and that of the ADP had some small peaks at specific frequencies (Fig. 5Ac) of the power spectra, but there was no peak for coherence above the β frequency (Fig. 5Ad, e). By postoperative day 14, however, both ADP and ED23 started showing oscillatory activity at around 30 Hz (Fig. 5Ba, b, c), although there was no coherence between them at this stage (Fig. 5Bd, e). Then on postoperative day 34–92, the 30-Hz oscillatory activities of these muscles were coupled (Fig. 5C and D), and the coherence between them increased further (Fig. 5Cd, e and 5Dd, e). Such IMC was widespread, occurring among a variety of hand/arm muscles, and not only between synergistic muscle pairs but also between antagonistic muscle pairs and between muscle pairs of various joints, including distal and proximal ones (Fig. 5E and F). The peak frequency of coherence was detected at 33.24 ± 0.34 Hz (mean ± SD; range, 30–46 Hz). In Monkey Be, the coupling between most muscle pairs continuously increased through postoperative day 92 and decreased in only two pairs (Fig. 5Ea, b). In Monkey Mu, by contrast, the coupling between most muscle pairs increased for some time during the first postoperative 1–2 months, but then decreased during the third month. Only the coupling between the ADP and ED23 muscles maintained a high degree of coherency throughout the recovery (Fig. 5Fa, b). Such γ-band oscillatory LFP activities and coherence with muscle activities were not found in either the contra- or ipsilesional M1 (see Fig. 3B–Da, b and d, e), or the contralesional PMv or S1 (data not shown). Cortical activity displayed oscillatory components at either the α-band (8–13 Hz) or β-band (14–30 Hz) frequencies; both are lower than 30 Hz. Therefore, the IMC at frequencies of 30–46 Hz, which emerged during the course of recovery, was highly likely independent of cortical oscillation.Figure 5


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

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

Oscillatory coupling of muscle pair (ED23 and ADP) activities recorded at various times before and after the l-CST lesion. (A–D) preoperatively (A), postoperative day 14 (B), postoperative day 34 (C) and postoperative day 92 (D). (a) The rectified EMG activity from ED23 (top) and ADP (bottom). Data obtained during the hold phase of precision grip in Monkey Be. (b and c) power spectra of ED23 and ADP, respectively. (d) Coherence between ED23 and ADP. In the coherence plots, the grey horizontal lines represent the 95% confidence limit (0.0125). (e) Cross-correlograms between ED23 and ADP. In cross-correlograms, the y-axes on the right and left sides indicate the absolute and relative values, respectively. The grey vertical lines in the cross-correlograms represent the zero-lag time. (E and F) Changes in the 30–46-Hz IMC during recovery in Monkey Be (E) and Monkey Mu (F). (a) Coupling between ED23 and a variety of other muscles (see inset). (b) Coupling between ADP and a variety of other muscles (see inset). n.s. in (a) and (b) indicates coherence values that were not significant. The grey horizontal lines in (a) and (b) represent the 95% confidence limit of coherence.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2664448&req=5

Figure 5: Oscillatory coupling of muscle pair (ED23 and ADP) activities recorded at various times before and after the l-CST lesion. (A–D) preoperatively (A), postoperative day 14 (B), postoperative day 34 (C) and postoperative day 92 (D). (a) The rectified EMG activity from ED23 (top) and ADP (bottom). Data obtained during the hold phase of precision grip in Monkey Be. (b and c) power spectra of ED23 and ADP, respectively. (d) Coherence between ED23 and ADP. In the coherence plots, the grey horizontal lines represent the 95% confidence limit (0.0125). (e) Cross-correlograms between ED23 and ADP. In cross-correlograms, the y-axes on the right and left sides indicate the absolute and relative values, respectively. The grey vertical lines in the cross-correlograms represent the zero-lag time. (E and F) Changes in the 30–46-Hz IMC during recovery in Monkey Be (E) and Monkey Mu (F). (a) Coupling between ED23 and a variety of other muscles (see inset). (b) Coupling between ADP and a variety of other muscles (see inset). n.s. in (a) and (b) indicates coherence values that were not significant. The grey horizontal lines in (a) and (b) represent the 95% confidence limit of coherence.
Mentions: In addition to the postoperative emergence of long-term synchrony, the EMG activities of muscles ADP and ED23 also became oscillatory and coherent. Prior to spinal cord lesions, the EMG activity of the ED23 muscle contained frequency components over a broad range (Fig. 5Ab) and that of the ADP had some small peaks at specific frequencies (Fig. 5Ac) of the power spectra, but there was no peak for coherence above the β frequency (Fig. 5Ad, e). By postoperative day 14, however, both ADP and ED23 started showing oscillatory activity at around 30 Hz (Fig. 5Ba, b, c), although there was no coherence between them at this stage (Fig. 5Bd, e). Then on postoperative day 34–92, the 30-Hz oscillatory activities of these muscles were coupled (Fig. 5C and D), and the coherence between them increased further (Fig. 5Cd, e and 5Dd, e). Such IMC was widespread, occurring among a variety of hand/arm muscles, and not only between synergistic muscle pairs but also between antagonistic muscle pairs and between muscle pairs of various joints, including distal and proximal ones (Fig. 5E and F). The peak frequency of coherence was detected at 33.24 ± 0.34 Hz (mean ± SD; range, 30–46 Hz). In Monkey Be, the coupling between most muscle pairs continuously increased through postoperative day 92 and decreased in only two pairs (Fig. 5Ea, b). In Monkey Mu, by contrast, the coupling between most muscle pairs increased for some time during the first postoperative 1–2 months, but then decreased during the third month. Only the coupling between the ADP and ED23 muscles maintained a high degree of coherency throughout the recovery (Fig. 5Fa, b). Such γ-band oscillatory LFP activities and coherence with muscle activities were not found in either the contra- or ipsilesional M1 (see Fig. 3B–Da, b and d, e), or the contralesional PMv or S1 (data not shown). Cortical activity displayed oscillatory components at either the α-band (8–13 Hz) or β-band (14–30 Hz) frequencies; both are lower than 30 Hz. Therefore, the IMC at frequencies of 30–46 Hz, which emerged during the course of recovery, was highly likely independent of cortical oscillation.Figure 5

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