Quantitative and qualitative comparison of corticospinal projections from the hand and arm area of the primary motor cortex in monkeys with spinal cord injury

Spinal cord injury (SCI) often disrupts the integrity of afferent (sensory) axons projecting through the spinal cord dorsal columns to the brain. Examinations of ascending sensory tracts, therefore, are critical for monitoring the extent of SCI and recovery processes. In this review, we discuss the most common electrophysiological techniques used to assess transmission of afferent inputs to the primary motor cortex (i.e., afferent input-induced facilitation and inhibition) and the somatosensory cortex [i.e., somatosensory evoked potentials (SSEPs), dermatomal SSEPs, and electrical perceptual thresholds] following human SCI. We discuss how afferent input modulates corticospinal excitability by involving cortical and spinal mechanisms depending on the timing of the effects, which need to be considered separately for upper and lower limb muscles. We argue that the time of arrival of afferent input onto the sensory and motor cortex is critical to consider in plasticity-induced protocols in humans with SCI. We also discuss how current sensory exams have been used to detect differences between control and SCI participants but might be less optimal to characterize the level and severity of injury. There is a need to conduct some of these electrophysiological examinations during functionally relevant behaviors to understand the contribution of impaired afferent inputs to the control, or lack of control, of movement. Thus the effects of transmission of afferent inputs to the brain need to be considered on multiple functions following human SCI.

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Forelimb Motor Skills Deficits Following Thoracic Spinal Cord Injury: Underlying Dopaminergic and Neural Oscillatory Changes in Rat Primary Motor Cortex

ASN NEURO ◽

10.1177/17590914211044000 ◽

2021 ◽

Vol 13 ◽

pp. 175909142110440

Author(s):

Omid Salimi ◽

Hamid Soltani Zangbar ◽

Soheila Hajizadeh Shadiabad ◽

Meysam Ghorbani ◽

Tahereh Ghadiri ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Motor Cortex ◽

Motor Skills ◽

Primary Motor Cortex ◽

Dopaminergic System ◽

Oscillatory Activity ◽

R And D ◽

Cord Injury ◽

Skills Learning

The loss of spinal sensorimotor pathways following spinal cord injury (SCI) can induce retrograde neurodegeneration in the primary motor cortex (M1). However, the effect of thoracic SCI on forelimb motor skills has not been studied clearly. So, herein we aimed to examine the effects of the thoracic SCI model on forelimb motor skills learning, parallel with dopaminergic and oscillatory changes in hindlimb and forelimb areas (HLA and FLA) of M1 in rats. Male Wistar rats were randomly subjected to laminectomy (Control) or contusion SCI at the thoracic (T10) level. Oscillatory activity and motor skills performance were evaluated for six consecutive days using local field potential (LFP) recording and skilled forelimb reaching task, respectively. Dopamine (DA) levels and expression of dopamine receptors (D1R and D2R) were determined in HLA and FLA by ELISA and western blotting. LFP recording results showed a sustained increase of LFP power in SCI rats compared with uninjured rats through skilled reaching training. Also, the SCI group had a lower reaching performance and learning rate in contrast to the Control group. Biochemical analysis of HLA and FLA showed a reduction in DA levels and expression of D1R and D2R after SCI. According to these findings, thoracic SCI causes aberrant changes in the oscillatory activity and dopaminergic system of M1, which are not restricted to HLA but also found in FLA accompanied by a deficit in forelimb motor skills performance. Summary statement: The reorganization of the primary motor cortex, following spinal cord injury, is not restricted to the hind limb area, and interestingly extends to the forelimb limb area, which appears as a dysfunctional change in oscillations and dopaminergic system, associated with a deficit in motor skills learning of forelimb.

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What is the functional relevance of reorganization in primary motor cortex after spinal cord injury?

Neurobiology of Disease ◽

10.1016/j.nbd.2018.09.009 ◽

2019 ◽

Vol 121 ◽

pp. 286-295 ◽

Cited By ~ 3

Author(s):

M.A. Urbin ◽

Dylan A. Royston ◽

Douglas J. Weber ◽

Michael L. Boninger ◽

Jennifer L. Collinger

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Motor Cortex ◽

Primary Motor Cortex ◽

Cord Injury ◽

Functional Relevance

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Spinal Cord Injury-Induced Changes in Encoding and Decoding of Bipedal Walking by Motor Cortical Ensembles

Brain Sciences ◽

10.3390/brainsci11091193 ◽

2021 ◽

Vol 11 (9) ◽

pp. 1193

Author(s):

Dingyin Hu ◽

Shirong Wang ◽

Bo Li ◽

Honghao Liu ◽

Jiping He

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Motor Cortex ◽

Primary Motor Cortex ◽

Cell Activity ◽

Neuronal Population ◽

Pharmacological Therapy ◽

Motor Recovery ◽

Bipedal Walking ◽

Cord Injury

Recent studies have shown that motor recovery following spinal cord injury (SCI) is task-specific. However, most consequential conclusions about locomotor functional recovery from SCI have been derived from quadrupedal locomotion paradigms. In this study, two monkeys were trained to perform a bipedal walking task, mimicking human walking, before and after T8 spinal cord hemisection. Importantly, there is no pharmacological therapy with nerve growth factor for monkeys after SCI; thus, in this study, the changes that occurred in the brain were spontaneous. The impairment of locomotion on the ipsilateral side was more severe than that on the contralateral side. We used information theory to analyze single-cell activity from the left primary motor cortex (M1), and results show that neuronal populations in the unilateral primary motor cortex gradually conveyed more information about the bilateral hindlimb muscle activities during the training of bipedal walking after SCI. We further demonstrated that, after SCI, progressively expanded information from the neuronal population reconstructed more accurate control of muscle activity. These results suggest that, after SCI, the unilateral primary motor cortex could gradually regain control of bilateral coordination and motor recovery and in turn enhance the performance of brain–machine interfaces.

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Optogenetic Neuronal Stimulation Promotes Functional Recovery After Spinal Cord Injury

Frontiers in Neuroscience ◽

10.3389/fnins.2021.640255 ◽

2021 ◽

Vol 15 ◽

Author(s):

Wei-wei Deng ◽

Guang-yan Wu ◽

Ling-xia Min ◽

Zhou Feng ◽

Hui Chen ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Motor Cortex ◽

Functional Recovery ◽

Primary Motor Cortex ◽

Motor Evoked Potentials ◽

Cell Types ◽

Treatment Method ◽

Cord Injury ◽

Tissue Recovery

Although spinal cord injury (SCI) is the main cause of disability worldwide, there is still no definite and effective treatment method for this condition. Our previous clinical trials confirmed that the increased excitability of the motor cortex was related to the functional prognosis of patients with SCI. However, it remains unclear which cell types in the motor cortex lead to the later functional recovery. Herein, we applied optogenetic technology to selectively activate glutamate neurons in the primary motor cortex and explore whether activation of glutamate neurons in the primary motor cortex can promote functional recovery after SCI in rats and the preliminary neural mechanisms involved. Our results showed that the activation of glutamate neurons in the motor cortex could significantly improve the motor function scores in rats, effectively shorten the incubation period of motor evoked potentials and increase motor potentials’ amplitude. In addition, hematoxylin-eosin staining and nerve fiber staining at the injured site showed that accurate activation of the primary motor cortex could effectively promote tissue recovery and neurofilament growth (GAP-43, NF) at the injured site of the spinal cord, while the content of some growth-related proteins (BDNF, NGF) at the injured site increased. These results suggested that selective activation of glutamate neurons in the primary motor cortex can promote functional recovery after SCI and may be of great significance for understanding the neural cell mechanism underlying functional recovery induced by motor cortex stimulation.

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Exercise Ameliorates Spinal Cord Injury by Changing DNA Methylation

Cells ◽

10.3390/cells10010143 ◽

2021 ◽

Vol 10 (1) ◽

pp. 143

Author(s):

Ganchimeg Davaa ◽

Jin Young Hong ◽

Tae Uk Kim ◽

Seong Jae Lee ◽

Seo Young Kim ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Motor Cortex ◽

Functional Recovery ◽

Treadmill Exercise ◽

Exercise Group ◽

Control Group ◽

Epigenetic Changes ◽

Cord Injury ◽

The Brain

Exercise training is a traditional method to maximize remaining function in patients with spinal cord injury (SCI), but the exact mechanism by which exercise promotes recovery after SCI has not been identified; whether exercise truly has a beneficial effect on SCI also remains unclear. Previously, we showed that epigenetic changes in the brain motor cortex occur after SCI and that a treatment leading to epigenetic modulation effectively promotes functional recovery after SCI. We aimed to determine how exercise induces functional improvement in rats subjected to SCI and whether epigenetic changes are engaged in the effects of exercise. A spinal cord contusion model was established in rats, which were then subjected to treadmill exercise for 12 weeks. We found that the size of the lesion cavity and the number of macrophages were decreased more in the exercise group than in the control group after 12 weeks of injury. Immunofluorescence and DNA dot blot analysis revealed that levels of 5-methylcytosine (5mC) and 5-hydroxymethylcytosine (5hmC) in the brain motor cortex were increased after exercise. Accordingly, the expression of ten-eleven translocation (Tet) family members (Tet1, Tet2, and Tet3) in the brain motor cortex also elevated. However, no macrophage polarization was induced by exercise. Locomotor function, including Basso, Beattie, and Bresnahan (BBB) and ladder scores, also improved in the exercise group compared to the control group. We concluded that treadmill exercise facilitates functional recovery in rats with SCI, and mechanistically epigenetic changes in the brain motor cortex may contribute to exercise-induced improvements.

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