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Brain Sciences
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Mechanisms of Neuromodulation and Rehabilitation after Spinal Cord Injury
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Mechanisms of Neuromodulation and Rehabilitation after Spinal Cord Injury

A special issue of Brain Sciences (ISSN 2076-3425). This special issue belongs to the section "Systems Neuroscience".

Deadline for manuscript submissions: closed (20 November 2020) | Viewed by 25407

Special Issue Editors

Dr. Igor A. Lavrov

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Guest Editor
Department of Neurology, Mayo Clinic, Rochester, MN 55905 USA
Interests: Neuromodulation; Spinal cord Injury; Neuroprosthetics; Neurorehabilitation; Motor control
Dr. Peter Grahn

E-Mail Website
Guest Editor
Rehabilitation Medicine Research Center, Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN 55905 USA
Interests: Spinal cord Injury; Neuromodulation; Neuroprosthetics; Neurorehabilitation; Motor control

Special Issue Information

Dear Colleagues,

Multiple studies have demonstrated that spinal cord neuromodulation, together with rehabilitation, enables volitional motor control of previously paralyzed motor functions in humans diagnosed with severe traumatic spinal cord injury. However, there is a limited understanding of the underlying electrophysiological mechanisms of action, and the neural structures of the spine, that integrate extrinsic neuromodulatory stimuli with intrinsic sensory inputs from the periphery as well as descending sub-functional motor command signals spanning the injury site. More specifically, the mechanisms of generating volitional control over tonic and rhythmic patterns of spinal motor outputs using epidural stimulation after spinal cord injury are generally unknown. Limited evidence has shed light on the spinal circuits involved in posture and locomotion and their reorganization after injury, nevertheless the role of different components and specific spinal pathways remain unclear. In response to this gap in scientific knowledge, we invite you to contribute your expertise via manuscript submission to a Special Issue of Brain Sciences titled: Mechanisms of Neuromodulation and Rehabilitation after Spinal Cord Injury. Through this Special Issue, we aim to advance the current understanding of the effects of spinal cord neuromodulation to restore functions after spinal cord injury via publication of cutting-edge research that focuses on the mechanisms involved in spinal cord reorganization after injury, and more specifically, insight into circuitry-level mechanisms that underlie spinal cord neuromodulation and neurorehabilitation.

Dr. Igor A. Lavrov
Dr. Peter Grahn
Guest Editors

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Brain Sciences is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2200 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • spinal cord injury
  • neuromodulation
  • rehabilitation
  • central pattern generator
  • neuroplasticity
  • spinal sensorimotor circuitry

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Published Papers (6 papers)

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Research

24 pages, 5370 KiB  
Article
Ipsi- and Contralateral Oligo- and Polysynaptic Reflexes in Humans Revealed by Low-Frequency Epidural Electrical Stimulation of the Lumbar Spinal Cord
by Ursula S. Hofstoetter, Simon M. Danner, Brigitta Freundl, Heinrich Binder, Peter Lackner and Karen Minassian
Brain Sci. 2021, 11(1), 112; https://doi.org/10.3390/brainsci11010112 - 16 Jan 2021
Cited by 6 | Viewed by 3810
Abstract
Epidural electrical stimulation (EES) applied over the human lumbosacral spinal cord provides access to afferent fibers from virtually all lower-extremity nerves. These afferents connect to spinal networks that play a pivotal role in the control of locomotion. Studying EES-evoked responses mediated through these [...] Read more.
Epidural electrical stimulation (EES) applied over the human lumbosacral spinal cord provides access to afferent fibers from virtually all lower-extremity nerves. These afferents connect to spinal networks that play a pivotal role in the control of locomotion. Studying EES-evoked responses mediated through these networks can identify some of their functional components. We here analyzed electromyographic (EMG) responses evoked by low-frequency (2–6 Hz) EES derived from eight individuals with chronic, motor complete spinal cord injury. We identified and separately analyzed three previously undescribed response types: first, crossed reflexes with onset latencies of ~55 ms evoked in the hamstrings; second, oligosynaptic reflexes within 50 ms post-stimulus superimposed on the monosynaptic posterior root-muscle reflexes in the flexor muscle tibialis anterior, but with higher thresholds and no rate-sensitive depression; third, polysynaptic responses with variable EMG shapes within 50–450 ms post-stimulus evoked in the tibialis anterior and triceps surae, some of which demonstrated consistent changes in latencies with graded EES. Our observations suggest the activation of commissural neurons, lumbar propriospinal interneurons, and components of the late flexion reflex circuits through group I and II proprioceptive afferent inputs. These potential neural underpinnings have all been related to spinal locomotion in experimental studies. Full article
(This article belongs to the Special Issue Mechanisms of Neuromodulation and Rehabilitation after Spinal Cord Injury)
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11 pages, 1623 KiB  
Article
Rostrocaudal Distribution of the C-Fos-Immunopositive Spinal Network Defined by Muscle Activity during Locomotion
by Natalia Merkulyeva, Vsevolod Lyakhovetskii, Aleksandr Veshchitskii, Oleg Gorskii and Pavel Musienko
Brain Sci. 2021, 11(1), 69; https://doi.org/10.3390/brainsci11010069 - 7 Jan 2021
Cited by 6 | Viewed by 6745
Abstract
The optimization of multisystem neurorehabilitation protocols including electrical spinal cord stimulation and multi-directional tasks training require understanding of underlying circuits mechanisms and distribution of the neuronal network over the spinal cord. In this study we compared the locomotor activity during forward and backward [...] Read more.
The optimization of multisystem neurorehabilitation protocols including electrical spinal cord stimulation and multi-directional tasks training require understanding of underlying circuits mechanisms and distribution of the neuronal network over the spinal cord. In this study we compared the locomotor activity during forward and backward stepping in eighteen adult decerebrated cats. Interneuronal spinal networks responsible for forward and backward stepping were visualized using the C-Fos technique. A bi-modal rostrocaudal distribution of C-Fos-immunopositive neurons over the lumbosacral spinal cord (peaks in the L4/L5 and L6/S1 segments) was revealed. These patterns were compared with motoneuronal pools using Vanderhorst and Holstege scheme; the location of the first peak was correspondent to the motoneurons of the hip flexors and knee extensors, an inter-peak drop was presumably attributed to the motoneurons controlling the adductor muscles. Both were better expressed in cats stepping forward and in parallel, electromyographic (EMG) activity of the hip flexor and knee extensors was higher, while EMG activity of the adductor was lower, during this locomotor mode. On the basis of the present data, which showed greater activity of the adductor muscles and the attributed interneuronal spinal network during backward stepping and according with data about greater demands on postural control systems during backward locomotion, we suppose that the locomotor networks for movements in opposite directions are at least partially different. Full article
(This article belongs to the Special Issue Mechanisms of Neuromodulation and Rehabilitation after Spinal Cord Injury)
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16 pages, 2219 KiB  
Article
Effects of Functional Electrical Stimulation Cycling of Different Duration on Viscoelastic and Electromyographic Properties of the Knee in Patients with Spinal Cord Injury
by Antonino Casabona, Maria Stella Valle, Claudio Dominante, Luca Laudani, Maria Pia Onesta and Matteo Cioni
Brain Sci. 2021, 11(1), 7; https://doi.org/10.3390/brainsci11010007 - 23 Dec 2020
Cited by 7 | Viewed by 2872
Abstract
The benefits of functional electrical stimulation during cycling (FES-cycling) have been ascertained following spinal cord injury. The instrumented pendulum test was applied to chronic paraplegic patients to investigate the effects of FES-cycling of different duration (20-min vs. 40-min) on biomechanical and electromyographic characterization [...] Read more.
The benefits of functional electrical stimulation during cycling (FES-cycling) have been ascertained following spinal cord injury. The instrumented pendulum test was applied to chronic paraplegic patients to investigate the effects of FES-cycling of different duration (20-min vs. 40-min) on biomechanical and electromyographic characterization of knee mobility. Seven adults with post-traumatic paraplegia attended two FES-cycling sessions, a 20-min and a 40-min one, in a random order. Knee angular excursion, stiffness and viscosity were measured using the pendulum test before and after each session. Surface electromyographic activity was recorded from the rectus femoris (RF) and biceps femoris (BF) muscles. FES-cycling led to reduced excursion (p < 0.001) and increased stiffness (p = 0.005) of the knee, which was more evident after the 20-min than 40-min session. Noteworthy, biomechanical changes were associated with an increase of muscle activity and changes in latency of muscle activity only for 20-min, with anticipated response times for RF (p < 0.001) and delayed responses for BF (p = 0.033). These results indicate that significant functional changes in knee mobility can be achieved by FES-cycling for 20 min, as evaluated by the pendulum test in patients with chronic paraplegia. The observed muscle behaviour suggests modulatory effects of exercise on spinal network aimed to partially restore automatic neuronal processes. Full article
(This article belongs to the Special Issue Mechanisms of Neuromodulation and Rehabilitation after Spinal Cord Injury)
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13 pages, 2675 KiB  
Article
Effects of Rehabilitation on Perineural Nets and Synaptic Plasticity Following Spinal Cord Transection
by Yazi D. Al’joboori, V. Reggie Edgerton and Ronaldo M. Ichiyama
Brain Sci. 2020, 10(11), 824; https://doi.org/10.3390/brainsci10110824 - 6 Nov 2020
Cited by 11 | Viewed by 3453
Abstract
Epidural electrical stimulation (ES) of the lumbar spinal cord combined with daily locomotor training has been demonstrated to enhance stepping ability after complete spinal transection in rodents and clinically complete spinal injuries in humans. Although functional gain is observed, plasticity mechanisms associated with [...] Read more.
Epidural electrical stimulation (ES) of the lumbar spinal cord combined with daily locomotor training has been demonstrated to enhance stepping ability after complete spinal transection in rodents and clinically complete spinal injuries in humans. Although functional gain is observed, plasticity mechanisms associated with such recovery remain mostly unclear. Here, we investigated how ES and locomotor training affected expression of chondroitin sulfate proteoglycans (CSPG), perineuronal nets (PNN), and synaptic plasticity on spinal motoneurons. To test this, adult rats received a complete spinal transection (T9–T10) followed by daily locomotor training performed under ES with administration of quipazine (a serotonin (5-HT) agonist) starting 7 days post-injury (dpi). Excitatory and inhibitory synaptic changes were examined at 7, 21, and 67 dpi in addition to PNN and CSPG expression. The total amount of CSPG expression significantly increased with time after injury, with no effect of training. An interesting finding was that γ-motoneurons did not express PNNs, whereas α-motoneurons demonstrated well-defined PNNs. This remarkable difference is reflected in the greater extent of synaptic changes observed in γ-motoneurons compared to α-motoneurons. A medium negative correlation between CSPG expression and changes in putative synapses around α-motoneurons was found, but no correlation was identified for γ-motoneurons. These results suggest that modulation of γ-motoneuron activity is an important mechanism associated with functional recovery induced by locomotor training under ES after a complete spinal transection. Full article
(This article belongs to the Special Issue Mechanisms of Neuromodulation and Rehabilitation after Spinal Cord Injury)
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15 pages, 1504 KiB  
Article
Combined Supra- and Sub-Lesional Epidural Electrical Stimulation for Restoration of the Motor Functions after Spinal Cord Injury in Mini Pigs
by Filip Fadeev, Anton Eremeev, Farid Bashirov, Roman Shevchenko, Andrei Izmailov, Vage Markosyan, Mikhail Sokolov, Julia Kalistratova, Anastasiia Khalitova, Ravil Garifulin, Rustem Islamov and Igor Lavrov
Brain Sci. 2020, 10(10), 744; https://doi.org/10.3390/brainsci10100744 - 16 Oct 2020
Cited by 13 | Viewed by 3915
Abstract
This study evaluates the effect of combined epidural electrical stimulation (EES) applied above (C5) and below (L2) the spinal cord injury (SCI) at T8–9 combined with motor training on the restoration of sensorimotor function in mini pigs. The motor evoked potentials (MEP) induced [...] Read more.
This study evaluates the effect of combined epidural electrical stimulation (EES) applied above (C5) and below (L2) the spinal cord injury (SCI) at T8–9 combined with motor training on the restoration of sensorimotor function in mini pigs. The motor evoked potentials (MEP) induced by EES applied at C5 and L2 levels were recorded in soleus muscles before and two weeks after SCI. EES treatment started two weeks after SCI and continued for 6 weeks led to improvement in multiple metrics, including behavioral, electrophysiological, and joint kinematics outcomes. In control animals after SCI a multiphasic M-response was observed during M/H-response testing, while animals received EES-enable training demonstrated the restoration of the M-response and H-reflex, although at a lower amplitude. The joint kinematic and assessment with Porcine Thoracic Injury Behavior scale (PTIBS) motor recovery scale demonstrated improvement in animals that received EES-enable training compared to animals with no treatment. The positive effect of two-level (cervical and lumbar) epidural electrical stimulation on functional restoration in mini pigs following spinal cord contusion injury in mini pigs could be related with facilitation of spinal circuitry at both levels and activation of multisegmental coordination. This approach can be taken as a basis for the future development of neuromodulation and neurorehabilitation therapy for patients with spinal cord injury. Full article
(This article belongs to the Special Issue Mechanisms of Neuromodulation and Rehabilitation after Spinal Cord Injury)
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10 pages, 1063 KiB  
Article
Activation of the Supplementary Motor Areas Enhances Spinal Reciprocal Inhibition in Healthy Individuals
by Ryo Hirabayashi, Sho Kojima, Mutsuaki Edama and Hideaki Onishi
Brain Sci. 2020, 10(9), 587; https://doi.org/10.3390/brainsci10090587 - 24 Aug 2020
Cited by 7 | Viewed by 3472
Abstract
The supplementary motor area (SMA) may modulate spinal reciprocal inhibition (RI) because the descending input from the SMA is coupled to interneurons in the spinal cord via the reticulospinal tract. Our study aimed to verify whether the anodal transcranial direct current stimulation (anodal-tDCS) [...] Read more.
The supplementary motor area (SMA) may modulate spinal reciprocal inhibition (RI) because the descending input from the SMA is coupled to interneurons in the spinal cord via the reticulospinal tract. Our study aimed to verify whether the anodal transcranial direct current stimulation (anodal-tDCS) of the SMA enhances RI. Two tDCS conditions were used: the anodal stimulation (anodal-tDCS) and sham stimulation (sham-tDCS) conditions. To measure RI, there were two conditions: one with the test stimulus (alone) and the other with the conditioning-test stimulation intervals (CTIs), including 2 ms and 20 ms. RI was calculated at multiple time points: before the tDCS intervention (Pre); at 5 (Int 5) and 10 min; and immediately after (Post 0); and at 5, 10 (Post 10), 15, and 20 min after the intervention. In anodal-tDCS, the amplitude values of H-reflex were significantly reduced for a CTI of 2 ms at Int 5 to Post 0, and a CTI of 20 ms at Int 5 to Pot 10 compared with Pre. Stimulation of the SMA with anodal-tDCS for 15 min activated inhibitory interneurons in RIs by descending input from the reticulospinal tract via cortico–reticulospinal projections. The results showed that 15 min of anodal-tDCS in the SMA enhanced and sustained RI in healthy individuals. Full article
(This article belongs to the Special Issue Mechanisms of Neuromodulation and Rehabilitation after Spinal Cord Injury)
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