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Simultaneous Brain-Cervical Cord fMRI Reveals Intrinsic Spinal Cord Plasticity during Motor Sequence Learning.

Vahdat S, Lungu O, Cohen-Adad J, Marchand-Pauvert V, Benali H, Doyon J - PLoS Biol. (2015)

Bottom Line: Specifically, we show learning-related modulation of activity in the C6-C8 spinal region, which is independent from that of related supraspinal sensorimotor structures.Moreover, a brain-spinal cord functional connectivity analysis demonstrates that the initial linear relationship between the spinal cord and sensorimotor cortex gradually fades away over the course of motor sequence learning, while the connectivity between spinal activity and cerebellum gains strength.The present findings open new avenues for rehabilitation of patients with spinal cord injuries, as they demonstrate that this part of the central nervous system is much more plastic than assumed before.

View Article: PubMed Central - PubMed

Affiliation: Functional Neuroimaging Unit, University of Montreal, Montreal, Quebec, Canada; SensoriMotor Rehabilitation Research Team (CIHR), Montreal, Canada.

ABSTRACT
The spinal cord participates in the execution of skilled movements by translating high-level cerebral motor representations into musculotopic commands. Yet, the extent to which motor skill acquisition relies on intrinsic spinal cord processes remains unknown. To date, attempts to address this question were limited by difficulties in separating spinal local effects from supraspinal influences through traditional electrophysiological and neuroimaging methods. Here, for the first time, we provide evidence for local learning-induced plasticity in intact human spinal cord through simultaneous functional magnetic resonance imaging of the brain and spinal cord during motor sequence learning. Specifically, we show learning-related modulation of activity in the C6-C8 spinal region, which is independent from that of related supraspinal sensorimotor structures. Moreover, a brain-spinal cord functional connectivity analysis demonstrates that the initial linear relationship between the spinal cord and sensorimotor cortex gradually fades away over the course of motor sequence learning, while the connectivity between spinal activity and cerebellum gains strength. These data suggest that the spinal cord not only constitutes an active functional component of the human motor learning network but also contributes distinctively from the brain to the learning process. The present findings open new avenues for rehabilitation of patients with spinal cord injuries, as they demonstrate that this part of the central nervous system is much more plastic than assumed before. Yet, the neurophysiological mechanisms underlying this intrinsic functional plasticity in the spinal cord warrant further investigations.

No MeSH data available.


Related in: MedlinePlus

Neural correlates of motor sequence learning.Distinct cortical, subcortical, and spinal clusters showed learning-related modulation in activity only during the CS condition. All clusters of activation are positively correlated with the performance speed. At the cortical level, the activation cluster was located in the contralateral sensorimotor cortex. At the subcortical level, one cluster was found in the contralateral putamen, while the other was observed in the ipsilateral lobule V-VI of the cerebellum. In the spinal cord, activation clusters were centered on the C7–C8 spinal segments, similar to those observed in the main effect of practice. The color bars indicate Z-score values; all activation maps are corrected for multiple comparisons using GRF, p < 0.01.
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pbio.1002186.g003: Neural correlates of motor sequence learning.Distinct cortical, subcortical, and spinal clusters showed learning-related modulation in activity only during the CS condition. All clusters of activation are positively correlated with the performance speed. At the cortical level, the activation cluster was located in the contralateral sensorimotor cortex. At the subcortical level, one cluster was found in the contralateral putamen, while the other was observed in the ipsilateral lobule V-VI of the cerebellum. In the spinal cord, activation clusters were centered on the C7–C8 spinal segments, similar to those observed in the main effect of practice. The color bars indicate Z-score values; all activation maps are corrected for multiple comparisons using GRF, p < 0.01.

Mentions: To test more specifically whether the observed cervical BOLD activity was modulated by the amount of motor learning in each subject, we sought to identify the neural correlates of improvement in performance speed using a repeated-measures general linear model. The results revealed that the amount of improvement in motor performance during the CS condition, but not the SS condition, was correlated with BOLD activity changes within two spinal cord clusters located at the same spinal level as those observed in the analysis looking at the main effect of practice (Fig 3, spinal level, corrected cluster-level p-values using GRF: p < 0.01 for both clusters). Here, the activity was primarily located bilaterally in the intermediate part of C7 and in the ipsilateral C8 region. Importantly, we also investigated the difference in modulation by performance speed across conditions (speed performance by condition interaction). Similar to the results of the CS modulation alone reported above (see Fig 3), this analysis resulted again in two significant activation clusters centered at the C7 and C8 spinal levels (S4 Fig), hence suggesting that, compared to the SS condition, the CS condition generated greater modulated activity during motor learning in these particular regions of the spinal cord. Finally, it is noteworthy that the performance speed was significantly increased in both CS and SS conditions over the course of learning (p<0.001 in both condition; Fig 1D). Thus, this suggests that the lack of modulation in spinal cord activity during the SS condition could not be due to a thresholding effect. This also suggests that motor speed change alone was insufficient to account for the activation changes observed in the spinal cord over the course of learning.


Simultaneous Brain-Cervical Cord fMRI Reveals Intrinsic Spinal Cord Plasticity during Motor Sequence Learning.

Vahdat S, Lungu O, Cohen-Adad J, Marchand-Pauvert V, Benali H, Doyon J - PLoS Biol. (2015)

Neural correlates of motor sequence learning.Distinct cortical, subcortical, and spinal clusters showed learning-related modulation in activity only during the CS condition. All clusters of activation are positively correlated with the performance speed. At the cortical level, the activation cluster was located in the contralateral sensorimotor cortex. At the subcortical level, one cluster was found in the contralateral putamen, while the other was observed in the ipsilateral lobule V-VI of the cerebellum. In the spinal cord, activation clusters were centered on the C7–C8 spinal segments, similar to those observed in the main effect of practice. The color bars indicate Z-score values; all activation maps are corrected for multiple comparisons using GRF, p < 0.01.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4488354&req=5

pbio.1002186.g003: Neural correlates of motor sequence learning.Distinct cortical, subcortical, and spinal clusters showed learning-related modulation in activity only during the CS condition. All clusters of activation are positively correlated with the performance speed. At the cortical level, the activation cluster was located in the contralateral sensorimotor cortex. At the subcortical level, one cluster was found in the contralateral putamen, while the other was observed in the ipsilateral lobule V-VI of the cerebellum. In the spinal cord, activation clusters were centered on the C7–C8 spinal segments, similar to those observed in the main effect of practice. The color bars indicate Z-score values; all activation maps are corrected for multiple comparisons using GRF, p < 0.01.
Mentions: To test more specifically whether the observed cervical BOLD activity was modulated by the amount of motor learning in each subject, we sought to identify the neural correlates of improvement in performance speed using a repeated-measures general linear model. The results revealed that the amount of improvement in motor performance during the CS condition, but not the SS condition, was correlated with BOLD activity changes within two spinal cord clusters located at the same spinal level as those observed in the analysis looking at the main effect of practice (Fig 3, spinal level, corrected cluster-level p-values using GRF: p < 0.01 for both clusters). Here, the activity was primarily located bilaterally in the intermediate part of C7 and in the ipsilateral C8 region. Importantly, we also investigated the difference in modulation by performance speed across conditions (speed performance by condition interaction). Similar to the results of the CS modulation alone reported above (see Fig 3), this analysis resulted again in two significant activation clusters centered at the C7 and C8 spinal levels (S4 Fig), hence suggesting that, compared to the SS condition, the CS condition generated greater modulated activity during motor learning in these particular regions of the spinal cord. Finally, it is noteworthy that the performance speed was significantly increased in both CS and SS conditions over the course of learning (p<0.001 in both condition; Fig 1D). Thus, this suggests that the lack of modulation in spinal cord activity during the SS condition could not be due to a thresholding effect. This also suggests that motor speed change alone was insufficient to account for the activation changes observed in the spinal cord over the course of learning.

Bottom Line: Specifically, we show learning-related modulation of activity in the C6-C8 spinal region, which is independent from that of related supraspinal sensorimotor structures.Moreover, a brain-spinal cord functional connectivity analysis demonstrates that the initial linear relationship between the spinal cord and sensorimotor cortex gradually fades away over the course of motor sequence learning, while the connectivity between spinal activity and cerebellum gains strength.The present findings open new avenues for rehabilitation of patients with spinal cord injuries, as they demonstrate that this part of the central nervous system is much more plastic than assumed before.

View Article: PubMed Central - PubMed

Affiliation: Functional Neuroimaging Unit, University of Montreal, Montreal, Quebec, Canada; SensoriMotor Rehabilitation Research Team (CIHR), Montreal, Canada.

ABSTRACT
The spinal cord participates in the execution of skilled movements by translating high-level cerebral motor representations into musculotopic commands. Yet, the extent to which motor skill acquisition relies on intrinsic spinal cord processes remains unknown. To date, attempts to address this question were limited by difficulties in separating spinal local effects from supraspinal influences through traditional electrophysiological and neuroimaging methods. Here, for the first time, we provide evidence for local learning-induced plasticity in intact human spinal cord through simultaneous functional magnetic resonance imaging of the brain and spinal cord during motor sequence learning. Specifically, we show learning-related modulation of activity in the C6-C8 spinal region, which is independent from that of related supraspinal sensorimotor structures. Moreover, a brain-spinal cord functional connectivity analysis demonstrates that the initial linear relationship between the spinal cord and sensorimotor cortex gradually fades away over the course of motor sequence learning, while the connectivity between spinal activity and cerebellum gains strength. These data suggest that the spinal cord not only constitutes an active functional component of the human motor learning network but also contributes distinctively from the brain to the learning process. The present findings open new avenues for rehabilitation of patients with spinal cord injuries, as they demonstrate that this part of the central nervous system is much more plastic than assumed before. Yet, the neurophysiological mechanisms underlying this intrinsic functional plasticity in the spinal cord warrant further investigations.

No MeSH data available.


Related in: MedlinePlus