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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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Cortico-muscular coupling recorded at various times before and after the l-CST lesion. (A) preoperatively; (B) postoperative day 13; (C) postoperative day 33; (D) postoperative day 92. (a) Power spectra of LFP in contralesional M1 hand area. (b) Coherence between LFP in contralesional M1 hand area and EMG of ADP in ipsilesional side. (c) Cross-correlogram between LFP in contralesional M1 hand area and EMG of ADP in ipsilesional side. (d) Power spectra of LFP in ipsilesional M1 hand area. (e) Coherence between LFP in ipsilesional M1 hand area and EMG of ADP in ipsilesional side. (f) cross-correlogram between LFP in ipsilesional M1 hand area and EMG of ADP in ipsilesional side. (g) Power spectra of EMG of ADP in ipsilesional side. Coherence and cross-correlation estimates in this figure were calculated during the hold phase of force production. In the coherence plots of (a) and (d), the grey horizontal lines represent the 95% confidence limit of 0.0125. The vertical grey lines in the cross-correlograms represent the zero-lag time. Data in this figure were obtained in Monkey Mu.
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Figure 3: Cortico-muscular coupling recorded at various times before and after the l-CST lesion. (A) preoperatively; (B) postoperative day 13; (C) postoperative day 33; (D) postoperative day 92. (a) Power spectra of LFP in contralesional M1 hand area. (b) Coherence between LFP in contralesional M1 hand area and EMG of ADP in ipsilesional side. (c) Cross-correlogram between LFP in contralesional M1 hand area and EMG of ADP in ipsilesional side. (d) Power spectra of LFP in ipsilesional M1 hand area. (e) Coherence between LFP in ipsilesional M1 hand area and EMG of ADP in ipsilesional side. (f) cross-correlogram between LFP in ipsilesional M1 hand area and EMG of ADP in ipsilesional side. (g) Power spectra of EMG of ADP in ipsilesional side. Coherence and cross-correlation estimates in this figure were calculated during the hold phase of force production. In the coherence plots of (a) and (d), the grey horizontal lines represent the 95% confidence limit of 0.0125. The vertical grey lines in the cross-correlograms represent the zero-lag time. Data in this figure were obtained in Monkey Mu.

Mentions: LFPs in bilateral M1 hand area and EMGs of various hand/arm muscles were simultaneously recorded during a preoperative force-tracking precision grip task and throughout the recovery (Fig. 1). In Monkey Mu, Fourier analysis revealed that the LFPs in the hand area of bilateral M1 included peaks of power at both α- (8–13 Hz) and β- (14–30 Hz) frequency bands (Fig. 3Aa, d) preoperatively. The peak at the β-band component was higher than that at the α-band in both hemispheres. During this time, the EMG activity of an intrinsic hand muscle (ADP) contained frequency components over a broad range (Fig. 3Ag). Coherence analysis of the LFP and the EMG showed clear CMC between the contralateral M1 and ADP at the β-band with a peak at 17 Hz (Fig. 3Ab, c), whereas no coherence was found between the ipsilateral M1 and ADP (Fig. 3Ae, f). During the first month after the l-CST lesion, the β-band oscillatory component of the LFP in M1 decreased, and the α-band component predominated instead (Fig. 3Ba, Ca). But by postoperative day 92, the β-band oscillation recovered (Fig. 3Da, d) on both sides. The EMG activities of ADP started showing oscillatory activity around 33 Hz, which is in γ-band range during recovery (Fig. 3Cg, Dg); however, the CMC disappeared completely and did not recover at all by postoperative day 92 (Fig. 3Bb, Cb, Db), when the ability of precision grip had already recovered (Fig. 2C). By comparison, in Monkey Be, although the M1 LFP showed oscillations at both the α- and β-bands before the lesion and during recovery (data not shown), no coupling was observed between LFP and EMG activity before lesion, as previously reported in some healthy human subjects (Kilner et al., 2000; Baker and Baker, 2003) and never emerged during recovery.Figure 3


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

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

Cortico-muscular coupling recorded at various times before and after the l-CST lesion. (A) preoperatively; (B) postoperative day 13; (C) postoperative day 33; (D) postoperative day 92. (a) Power spectra of LFP in contralesional M1 hand area. (b) Coherence between LFP in contralesional M1 hand area and EMG of ADP in ipsilesional side. (c) Cross-correlogram between LFP in contralesional M1 hand area and EMG of ADP in ipsilesional side. (d) Power spectra of LFP in ipsilesional M1 hand area. (e) Coherence between LFP in ipsilesional M1 hand area and EMG of ADP in ipsilesional side. (f) cross-correlogram between LFP in ipsilesional M1 hand area and EMG of ADP in ipsilesional side. (g) Power spectra of EMG of ADP in ipsilesional side. Coherence and cross-correlation estimates in this figure were calculated during the hold phase of force production. In the coherence plots of (a) and (d), the grey horizontal lines represent the 95% confidence limit of 0.0125. The vertical grey lines in the cross-correlograms represent the zero-lag time. Data in this figure were obtained in Monkey Mu.
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Figure 3: Cortico-muscular coupling recorded at various times before and after the l-CST lesion. (A) preoperatively; (B) postoperative day 13; (C) postoperative day 33; (D) postoperative day 92. (a) Power spectra of LFP in contralesional M1 hand area. (b) Coherence between LFP in contralesional M1 hand area and EMG of ADP in ipsilesional side. (c) Cross-correlogram between LFP in contralesional M1 hand area and EMG of ADP in ipsilesional side. (d) Power spectra of LFP in ipsilesional M1 hand area. (e) Coherence between LFP in ipsilesional M1 hand area and EMG of ADP in ipsilesional side. (f) cross-correlogram between LFP in ipsilesional M1 hand area and EMG of ADP in ipsilesional side. (g) Power spectra of EMG of ADP in ipsilesional side. Coherence and cross-correlation estimates in this figure were calculated during the hold phase of force production. In the coherence plots of (a) and (d), the grey horizontal lines represent the 95% confidence limit of 0.0125. The vertical grey lines in the cross-correlograms represent the zero-lag time. Data in this figure were obtained in Monkey Mu.
Mentions: LFPs in bilateral M1 hand area and EMGs of various hand/arm muscles were simultaneously recorded during a preoperative force-tracking precision grip task and throughout the recovery (Fig. 1). In Monkey Mu, Fourier analysis revealed that the LFPs in the hand area of bilateral M1 included peaks of power at both α- (8–13 Hz) and β- (14–30 Hz) frequency bands (Fig. 3Aa, d) preoperatively. The peak at the β-band component was higher than that at the α-band in both hemispheres. During this time, the EMG activity of an intrinsic hand muscle (ADP) contained frequency components over a broad range (Fig. 3Ag). Coherence analysis of the LFP and the EMG showed clear CMC between the contralateral M1 and ADP at the β-band with a peak at 17 Hz (Fig. 3Ab, c), whereas no coherence was found between the ipsilateral M1 and ADP (Fig. 3Ae, f). During the first month after the l-CST lesion, the β-band oscillatory component of the LFP in M1 decreased, and the α-band component predominated instead (Fig. 3Ba, Ca). But by postoperative day 92, the β-band oscillation recovered (Fig. 3Da, d) on both sides. The EMG activities of ADP started showing oscillatory activity around 33 Hz, which is in γ-band range during recovery (Fig. 3Cg, Dg); however, the CMC disappeared completely and did not recover at all by postoperative day 92 (Fig. 3Bb, Cb, Db), when the ability of precision grip had already recovered (Fig. 2C). By comparison, in Monkey Be, although the M1 LFP showed oscillations at both the α- and β-bands before the lesion and during recovery (data not shown), no coupling was observed between LFP and EMG activity before lesion, as previously reported in some healthy human subjects (Kilner et al., 2000; Baker and Baker, 2003) and never emerged during recovery.Figure 3

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