Limits...
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 practice in the spinal cord.(A) Activation maps representing the main effect of practice during the CS (red) and SS (blue) conditions are overlaid on the structural image of a reference subject. The yellow box indicates the sagittal section (x = -2.6 mm left), and the oblique yellow lines indicate the location of different transversal sections that are then displayed on the left and right sides of the figure. Note that the peaks of BOLD responses in both conditions are centered on the C7 spinal segment, mostly ipsilateral to the side of finger movements. The upper plots illustrate the percent change of the BOLD signal, averaged across blocks and subjects, during the CS (red) and the SS (blue) conditions. For averaging purposes, the BOLD signal of each block was resampled to obtain an equal number of points per block. The bright gray box represents the average duration of each block. The shaded area represents SEM; the color bars indicate Z-score values; all activation maps are corrected for multiple comparisons using GRF, p < 0.01. (B) There is a significant difference in mean amplitude of the BOLD signal change between the CS and SS conditions. (C) Similarly, the spatial extent of activation within the C6–C8 spinal segments is significantly larger in the CS as compared to the SS condition. Error bars represent SEM; * indicates p<0.05.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4488354&req=5

pbio.1002186.g002: Neural correlates of motor practice in the spinal cord.(A) Activation maps representing the main effect of practice during the CS (red) and SS (blue) conditions are overlaid on the structural image of a reference subject. The yellow box indicates the sagittal section (x = -2.6 mm left), and the oblique yellow lines indicate the location of different transversal sections that are then displayed on the left and right sides of the figure. Note that the peaks of BOLD responses in both conditions are centered on the C7 spinal segment, mostly ipsilateral to the side of finger movements. The upper plots illustrate the percent change of the BOLD signal, averaged across blocks and subjects, during the CS (red) and the SS (blue) conditions. For averaging purposes, the BOLD signal of each block was resampled to obtain an equal number of points per block. The bright gray box represents the average duration of each block. The shaded area represents SEM; the color bars indicate Z-score values; all activation maps are corrected for multiple comparisons using GRF, p < 0.01. (B) There is a significant difference in mean amplitude of the BOLD signal change between the CS and SS conditions. (C) Similarly, the spatial extent of activation within the C6–C8 spinal segments is significantly larger in the CS as compared to the SS condition. Error bars represent SEM; * indicates p<0.05.

Mentions: We first assessed fMRI correlates of motor practice during the SS (blue) and CS (red) conditions compared to the baseline rest periods in the brain and cervical cord separately using two repeated measures general linear models (GLM) at the group level. All the brain and spinal cord group-level activation maps were corrected for multiple comparisons using Gaussian random field (GRF) theory correction. As expected at the brain level, similar sensorimotor regions as previously reported (cerebellum, putamen, supplementary motor area, premotor and primary sensorimotor cortices) were activated during the CS and SS conditions (S1 Fig) [1,2,4]. Most importantly, however, greater blood oxygenated level–dependent (BOLD) activity was also found at the expected C6–C8 spinal levels of the cervical cord, wherein motoneurons innervating the finger muscles reside, during performance of the CS and SS conditions (Fig 2A; main effect of practice, corrected cluster-level p-values using GRF: p < 0.0001 for CS and p = 0.001 for SS condition). Also as expected, BOLD activity in this spinal cord region was mostly located on the side ipsilateral to the hand (left) used to perform the tasks. As shown in Fig 2A, group-level activated regions related to the main effect of practice during the CS and SS conditions were almost overlapping (i.e., peaks of activity in both conditions were located ipsilaterally at the C6–C8 spinal level). However, critically, individual subject’s activation maps related to the CS condition (S2 Fig) also revealed that 21 out of 23 subjects showed a consistent cluster of activity in that same region, hence demonstrating the robustness of this pattern of activity at the spinal cord level. Furthermore, since the activation maps were largely overlapping between the two conditions, a direct comparison between them did not result in any significant cluster at the group level using the applied family-wise corrected threshold.


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 practice in the spinal cord.(A) Activation maps representing the main effect of practice during the CS (red) and SS (blue) conditions are overlaid on the structural image of a reference subject. The yellow box indicates the sagittal section (x = -2.6 mm left), and the oblique yellow lines indicate the location of different transversal sections that are then displayed on the left and right sides of the figure. Note that the peaks of BOLD responses in both conditions are centered on the C7 spinal segment, mostly ipsilateral to the side of finger movements. The upper plots illustrate the percent change of the BOLD signal, averaged across blocks and subjects, during the CS (red) and the SS (blue) conditions. For averaging purposes, the BOLD signal of each block was resampled to obtain an equal number of points per block. The bright gray box represents the average duration of each block. The shaded area represents SEM; the color bars indicate Z-score values; all activation maps are corrected for multiple comparisons using GRF, p < 0.01. (B) There is a significant difference in mean amplitude of the BOLD signal change between the CS and SS conditions. (C) Similarly, the spatial extent of activation within the C6–C8 spinal segments is significantly larger in the CS as compared to the SS condition. Error bars represent SEM; * indicates p<0.05.
© Copyright Policy
Related In: Results  -  Collection

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

pbio.1002186.g002: Neural correlates of motor practice in the spinal cord.(A) Activation maps representing the main effect of practice during the CS (red) and SS (blue) conditions are overlaid on the structural image of a reference subject. The yellow box indicates the sagittal section (x = -2.6 mm left), and the oblique yellow lines indicate the location of different transversal sections that are then displayed on the left and right sides of the figure. Note that the peaks of BOLD responses in both conditions are centered on the C7 spinal segment, mostly ipsilateral to the side of finger movements. The upper plots illustrate the percent change of the BOLD signal, averaged across blocks and subjects, during the CS (red) and the SS (blue) conditions. For averaging purposes, the BOLD signal of each block was resampled to obtain an equal number of points per block. The bright gray box represents the average duration of each block. The shaded area represents SEM; the color bars indicate Z-score values; all activation maps are corrected for multiple comparisons using GRF, p < 0.01. (B) There is a significant difference in mean amplitude of the BOLD signal change between the CS and SS conditions. (C) Similarly, the spatial extent of activation within the C6–C8 spinal segments is significantly larger in the CS as compared to the SS condition. Error bars represent SEM; * indicates p<0.05.
Mentions: We first assessed fMRI correlates of motor practice during the SS (blue) and CS (red) conditions compared to the baseline rest periods in the brain and cervical cord separately using two repeated measures general linear models (GLM) at the group level. All the brain and spinal cord group-level activation maps were corrected for multiple comparisons using Gaussian random field (GRF) theory correction. As expected at the brain level, similar sensorimotor regions as previously reported (cerebellum, putamen, supplementary motor area, premotor and primary sensorimotor cortices) were activated during the CS and SS conditions (S1 Fig) [1,2,4]. Most importantly, however, greater blood oxygenated level–dependent (BOLD) activity was also found at the expected C6–C8 spinal levels of the cervical cord, wherein motoneurons innervating the finger muscles reside, during performance of the CS and SS conditions (Fig 2A; main effect of practice, corrected cluster-level p-values using GRF: p < 0.0001 for CS and p = 0.001 for SS condition). Also as expected, BOLD activity in this spinal cord region was mostly located on the side ipsilateral to the hand (left) used to perform the tasks. As shown in Fig 2A, group-level activated regions related to the main effect of practice during the CS and SS conditions were almost overlapping (i.e., peaks of activity in both conditions were located ipsilaterally at the C6–C8 spinal level). However, critically, individual subject’s activation maps related to the CS condition (S2 Fig) also revealed that 21 out of 23 subjects showed a consistent cluster of activity in that same region, hence demonstrating the robustness of this pattern of activity at the spinal cord level. Furthermore, since the activation maps were largely overlapping between the two conditions, a direct comparison between them did not result in any significant cluster at the group level using the applied family-wise corrected threshold.

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