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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

Behavioral and imaging protocols.(A) The complex (CS; 4-1-3-2-4) and simple (SS; 4-3-2-1) motor sequence learning tasks were executed with the left (nondominant) hand. Subjects were required to execute 12 CS and 12 SS blocks of practice, with 60 movements each. (B) The CS and SS conditions were split evenly across blocks and alternated in a pseudorandom fashion. A 15-s rest period preceded and followed each block. (C) Functional axial slices (displayed here over the anatomical image of a representative subject) were acquired and covered both brain and cervical spinal cord up to the first thoracic (T1) segment, and they were placed at an angle that was perpendicular to the C4 vertebral segment. (D) Performance speeds (i.e., block duration) averaged across all subjects show that the learning curves differed between the CS (red) and SS (blue) conditions. Participants reached asymptotic performance after the fourth block in the SS and after the eighth block in the CS condition. (E) Learning index (mean duration of the last two blocks subtracted from the first two blocks’ mean) revealed a significant difference in performance between the CS and SS conditions. Error bars represent standard error of the mean (SEM); * indicates p<0.05.
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pbio.1002186.g001: Behavioral and imaging protocols.(A) The complex (CS; 4-1-3-2-4) and simple (SS; 4-3-2-1) motor sequence learning tasks were executed with the left (nondominant) hand. Subjects were required to execute 12 CS and 12 SS blocks of practice, with 60 movements each. (B) The CS and SS conditions were split evenly across blocks and alternated in a pseudorandom fashion. A 15-s rest period preceded and followed each block. (C) Functional axial slices (displayed here over the anatomical image of a representative subject) were acquired and covered both brain and cervical spinal cord up to the first thoracic (T1) segment, and they were placed at an angle that was perpendicular to the C4 vertebral segment. (D) Performance speeds (i.e., block duration) averaged across all subjects show that the learning curves differed between the CS (red) and SS (blue) conditions. Participants reached asymptotic performance after the fourth block in the SS and after the eighth block in the CS condition. (E) Learning index (mean duration of the last two blocks subtracted from the first two blocks’ mean) revealed a significant difference in performance between the CS and SS conditions. Error bars represent standard error of the mean (SEM); * indicates p<0.05.

Mentions: For the first time, we used functional magnetic resonance imaging (fMRI) to test the hypothesis that human spinal cord activity at the cervical level shows intrinsic learning-related changes during motor sequence learning (MSL). To do so, we acquired simultaneous images of the entire brain and cervical spinal cord during performance of a motor sequence task in healthy young subjects (Fig 1A–1C). A well-known MSL paradigm was chosen so that we could then link the novel imaging findings found here at the spinal cord level to the well-established behavioral determinants and neural correlates of MSL at the brain level (e.g., see [2,17], for reviews). This allowed us to examine the relative contribution of cortical, subcortical, and spinal regions in modulating performance during the early acquisition phase of a new sequence of movements and to investigate the functional connectivity between these structures over the course of motor 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)

Behavioral and imaging protocols.(A) The complex (CS; 4-1-3-2-4) and simple (SS; 4-3-2-1) motor sequence learning tasks were executed with the left (nondominant) hand. Subjects were required to execute 12 CS and 12 SS blocks of practice, with 60 movements each. (B) The CS and SS conditions were split evenly across blocks and alternated in a pseudorandom fashion. A 15-s rest period preceded and followed each block. (C) Functional axial slices (displayed here over the anatomical image of a representative subject) were acquired and covered both brain and cervical spinal cord up to the first thoracic (T1) segment, and they were placed at an angle that was perpendicular to the C4 vertebral segment. (D) Performance speeds (i.e., block duration) averaged across all subjects show that the learning curves differed between the CS (red) and SS (blue) conditions. Participants reached asymptotic performance after the fourth block in the SS and after the eighth block in the CS condition. (E) Learning index (mean duration of the last two blocks subtracted from the first two blocks’ mean) revealed a significant difference in performance between the CS and SS conditions. Error bars represent standard error of the mean (SEM); * indicates p<0.05.
© Copyright Policy
Related In: Results  -  Collection

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

pbio.1002186.g001: Behavioral and imaging protocols.(A) The complex (CS; 4-1-3-2-4) and simple (SS; 4-3-2-1) motor sequence learning tasks were executed with the left (nondominant) hand. Subjects were required to execute 12 CS and 12 SS blocks of practice, with 60 movements each. (B) The CS and SS conditions were split evenly across blocks and alternated in a pseudorandom fashion. A 15-s rest period preceded and followed each block. (C) Functional axial slices (displayed here over the anatomical image of a representative subject) were acquired and covered both brain and cervical spinal cord up to the first thoracic (T1) segment, and they were placed at an angle that was perpendicular to the C4 vertebral segment. (D) Performance speeds (i.e., block duration) averaged across all subjects show that the learning curves differed between the CS (red) and SS (blue) conditions. Participants reached asymptotic performance after the fourth block in the SS and after the eighth block in the CS condition. (E) Learning index (mean duration of the last two blocks subtracted from the first two blocks’ mean) revealed a significant difference in performance between the CS and SS conditions. Error bars represent standard error of the mean (SEM); * indicates p<0.05.
Mentions: For the first time, we used functional magnetic resonance imaging (fMRI) to test the hypothesis that human spinal cord activity at the cervical level shows intrinsic learning-related changes during motor sequence learning (MSL). To do so, we acquired simultaneous images of the entire brain and cervical spinal cord during performance of a motor sequence task in healthy young subjects (Fig 1A–1C). A well-known MSL paradigm was chosen so that we could then link the novel imaging findings found here at the spinal cord level to the well-established behavioral determinants and neural correlates of MSL at the brain level (e.g., see [2,17], for reviews). This allowed us to examine the relative contribution of cortical, subcortical, and spinal regions in modulating performance during the early acquisition phase of a new sequence of movements and to investigate the functional connectivity between these structures over the course of motor 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