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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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Schematic illustrations of the proposed mechanisms underlying functional recovery after the l-CST lesion, proposed from the present results. (A) In the intact state, a direct CM connection (black) or peripheral feedback (green) contributes to generate the cortico-muscular coupling at the frequency of the β-band. (B) During the recovery from l-CST lesion, subcortical neural systems (red) that mediate cortical command or peripheral feedback (green) to motoneurons might be involved in generating the 30–46-Hz IMC that emerged in a variety of hand/arm muscles. Dotted lines indicate polysynaptic connections.
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Figure 6: Schematic illustrations of the proposed mechanisms underlying functional recovery after the l-CST lesion, proposed from the present results. (A) In the intact state, a direct CM connection (black) or peripheral feedback (green) contributes to generate the cortico-muscular coupling at the frequency of the β-band. (B) During the recovery from l-CST lesion, subcortical neural systems (red) that mediate cortical command or peripheral feedback (green) to motoneurons might be involved in generating the 30–46-Hz IMC that emerged in a variety of hand/arm muscles. Dotted lines indicate polysynaptic connections.

Mentions: On the basis of these findings, as shown in Fig. 6, we propose that the γ-band-IMC, which emerges during recovery, represents an increasing common drive from subcortical neuronal systems and/or peripheral afferents to various spinal motoneuron pools. The neuronal substrate of such a ‘common subcortical oscillator’ is not clear at this moment. The interneuronal systems mediating indirect CM drive and/or reflex afferents from the periphery, which remained after the lesion, may possibly contribute to its generation. Because the coherence appears only when movements are voluntarily driven, the common subcortical oscillator might also be driven by descending inputs from the cerebral cortex and/or by peripheral feedback associated with the movement. They might include (i) propriospinal neurons with cell bodies in the C3–C4 segments and with axons passing through the ventral part of the lateral funiculus towards hand/arm muscle motoneurons (Alstermark et al., 1999; Isa et al., 2006), (ii) reticulospinal neurons that control both proximal and distal hand/arm muscles (Davidson and Buford, 2006; Davidson et al., 2007) and (iii) the subcortical reflex pathways through the brainstem or spinal cord.Figure 6


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

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

Schematic illustrations of the proposed mechanisms underlying functional recovery after the l-CST lesion, proposed from the present results. (A) In the intact state, a direct CM connection (black) or peripheral feedback (green) contributes to generate the cortico-muscular coupling at the frequency of the β-band. (B) During the recovery from l-CST lesion, subcortical neural systems (red) that mediate cortical command or peripheral feedback (green) to motoneurons might be involved in generating the 30–46-Hz IMC that emerged in a variety of hand/arm muscles. Dotted lines indicate polysynaptic connections.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

Figure 6: Schematic illustrations of the proposed mechanisms underlying functional recovery after the l-CST lesion, proposed from the present results. (A) In the intact state, a direct CM connection (black) or peripheral feedback (green) contributes to generate the cortico-muscular coupling at the frequency of the β-band. (B) During the recovery from l-CST lesion, subcortical neural systems (red) that mediate cortical command or peripheral feedback (green) to motoneurons might be involved in generating the 30–46-Hz IMC that emerged in a variety of hand/arm muscles. Dotted lines indicate polysynaptic connections.
Mentions: On the basis of these findings, as shown in Fig. 6, we propose that the γ-band-IMC, which emerges during recovery, represents an increasing common drive from subcortical neuronal systems and/or peripheral afferents to various spinal motoneuron pools. The neuronal substrate of such a ‘common subcortical oscillator’ is not clear at this moment. The interneuronal systems mediating indirect CM drive and/or reflex afferents from the periphery, which remained after the lesion, may possibly contribute to its generation. Because the coherence appears only when movements are voluntarily driven, the common subcortical oscillator might also be driven by descending inputs from the cerebral cortex and/or by peripheral feedback associated with the movement. They might include (i) propriospinal neurons with cell bodies in the C3–C4 segments and with axons passing through the ventral part of the lateral funiculus towards hand/arm muscle motoneurons (Alstermark et al., 1999; Isa et al., 2006), (ii) reticulospinal neurons that control both proximal and distal hand/arm muscles (Davidson and Buford, 2006; Davidson et al., 2007) and (iii) the subcortical reflex pathways through the brainstem or spinal cord.Figure 6

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