Altered modulation of sensorimotor rhythms with chronic paralysis

After paralysis, the disconnection between the cortex and its peripheral targets leads to neuroplasticity throughout the nervous system. However, it is unclear how chronic paralysis specifically impacts cortical oscillations associated with attempted movement of impaired limbs. We hypothesized that μ- (8–13 Hz) and β- (15–30 Hz) event-related desynchronization (ERD) would be less modulated for individuals with hand paralysis due to cervical spinal cord injury (SCI). To test this, we compared the modulation of ERD from magnetoencephalography (MEG) during attempted and imagined grasping performed by participants with cervical SCI ( n = 12) and able-bodied controls ( n = 13). Seven participants with tetraplegia were able to generate some electromyography (EMG) activity during attempted grasping, whereas the other five were not. The peak and area of ERD were significantly decreased for individuals without volitional muscle activity when they attempted to grasp compared with able-bodied subjects and participants with SCI,with some residual EMG activity. However, no significant differences were found between subject groups during mentally simulated tasks (i.e., motor imagery) where no muscle activity or somatosensory consequences were expected. These findings suggest that individuals who are unable to produce muscle activity are capable of generating ERD when attempting to move, but the characteristics of this ERD are altered. However, for people who maintain volitional muscle activity after SCI, there are no significant differences in ERD characteristics compared with able-bodied controls. These results provide evidence that ERD is dependent on the level of intact muscle activity after SCI. NEW & NOTEWORTHY Source space MEG was used to investigate sensorimotor cortical oscillations in individuals with SCI. This study provides evidence that individuals with cervical SCI exhibit decreased ERD when they attempt to grasp if they are incapable of generating muscle activity. However, there were no significant differences in ERD between paralyzed and able-bodied participants during motor imagery. These results have important implications for the design and evaluation of new therapies, such as motor imagery and neurofeedback interventions.

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Impact of glutamatergic and serotonergic neurotransmission on diaphragm muscle activity after cervical spinal hemisection

Journal of Neurophysiology ◽

10.1152/jn.00345.2017 ◽

2017 ◽

Vol 118 (3) ◽

pp. 1732-1738 ◽

Cited By ~ 8

Author(s):

Carlos B. Mantilla ◽

Heather M. Gransee ◽

Wen-Zhi Zhan ◽

Gary C. Sieck

Keyword(s):

Spinal Cord ◽

Nmda Receptor ◽

Muscle Activity ◽

Spontaneous Recovery ◽

Cervical Spinal Cord ◽

Diaphragm Muscle ◽

Emg Activity ◽

Emg Amplitude ◽

Cord Injury ◽

Phrenic Motoneuron

Incomplete cervical spinal cord hemisection at C2 (SH) disrupts descending excitatory drive to phrenic motoneurons, paralyzing the ipsilateral diaphragm muscle. Spontaneous recovery over time is associated with increased phrenic motoneuron expression of glutamatergic N-methyl-d-aspartate (NMDA) and serotonergic 5-HT2A receptors. We hypothesized that NMDA and 5-HT2A receptor-mediated neurotransmission play a role in ipsilateral diaphragm muscle activity post-SH. Adult male Sprague-Dawley rats were implanted with bilateral diaphragm EMG electrodes for chronic EMG recordings up to 28 days post-SH (SH 28D). The extent of recovery was calculated by peak root-mean-square (RMS) EMG amplitude. In all animals, absence of ipsilateral activity was verified at 3 days post-SH. Diaphragm EMG activity was also recorded during exposure to hypoxia-hypercapnia (10% O2-5% CO2). In SH animals displaying recovery of ipsilateral diaphragm EMG activity at SH 28D, cervical spinal cord segments containing the phrenic motor nucleus (C3–C5) were surgically exposed and either the NMDA receptor antagonist d-2-amino-5-phosphonovalerate (d-AP5; 100 mM, 30 μl) or 5-HT2A receptor antagonist ketanserin (40 mM, 30 μl) was instilled intrathecally. Following d-AP5, diaphragm EMG amplitude was reduced ipsilaterally, during both eupnea (42% of pre-d-AP5 value; P = 0.007) and hypoxia-hypercapnia (31% of pre-d-AP5 value; P = 0.015), with no effect on contralateral EMG activity or in uninjured controls. Treatment with ketanserin did not change ipsilateral or contralateral RMS EMG amplitude in SH animals displaying recovery at SH 28D. Our results suggest that spinal glutamatergic NMDA receptor-mediated neurotransmission plays an important role in ipsilateral diaphragm muscle activity after cervical spinal cord injury. NEW & NOTEWORTHY Spontaneous recovery following C2 spinal hemisection (SH) is associated with increased phrenic motoneuron expression of glutamatergic and serotonergic receptors. In this study, we show that pharmacological inhibition of glutamatergic N-methyl-d-aspartate (NMDA) receptors blunts ipsilateral diaphragm activity post-SH. In contrast, pharmacological inhibition of serotonergic 5-HT2A receptors does not change diaphragm EMG activity post-SH. Our results suggest that NMDA receptor-mediated glutamatergic neurotransmission plays an important role in enhancing rhythmic respiratory-related diaphragm activity after spinal cord injury.

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Tidal volume and diaphragm muscle activity in rats with cervical spinal cord injury

Journal of Physical Therapy Science ◽

10.1589/jpts.27.791 ◽

2015 ◽

Vol 27 (3) ◽

pp. 791-794 ◽

Cited By ~ 1

Author(s):

Hidetaka Imagita ◽

Akira Nishikawa ◽

Susumu Sakata ◽

Yasue Nishii ◽

Akira Minematsu ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Tidal Volume ◽

Muscle Activity ◽

Cervical Spinal Cord ◽

Cervical Spinal Cord Injury ◽

Diaphragm Muscle ◽

Cord Injury

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Muscle activity and mood state during simulated plant factory work in individuals with cervical spinal cord injury

Journal of Physical Therapy Science ◽

10.1589/jpts.28.881 ◽

2016 ◽

Vol 28 (3) ◽

pp. 881-885 ◽

Cited By ~ 1

Author(s):

Satoshi Okahara ◽

Masataka Kataoka ◽

Kuniharu Okuda ◽

Masato Shima ◽

Keiko Miyagaki ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Muscle Activity ◽

Mood State ◽

Cervical Spinal Cord ◽

Cervical Spinal Cord Injury ◽

Cord Injury ◽

Plant Factory

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Modulation of the extrinsic tongue muscle activity in response to bronchopulmonary C-fiber activation following midcervical contusion in the rat

Journal of Applied Physiology ◽

10.1152/japplphysiol.00857.2019 ◽

2020 ◽

Vol 128 (5) ◽

pp. 1130-1145

Author(s):

Hsiao-Sen Chang ◽

Kun-Ze Lee

Keyword(s):

Spinal Cord ◽

Muscle Activity ◽

Cervical Spinal Cord ◽

Upper Airway ◽

Airway Patency ◽

Tongue Muscle ◽

Cord Injury ◽

Burst Amplitude ◽

C Fiber ◽

Spinal Cord Contusion

Tongue muscle activity plays an important role in the regulation of upper airway patency. This study aimed to investigate the respiratory activity of the extrinsic tongue muscle in response to capsaicin-induced bronchopulmonary C-fiber activation following cervical spinal cord contusion. Midcervical spinal-contused animals exhibited a greater baseline preinspiratory burst amplitude of the extrinsic tongue muscle and were resistant to inhaled capsaicin-induced reduction of respiratory tongue muscle activity at the acute injured stage. However, inhalation of capsaicin caused a more severe attenuation of preinspiratory activity of the extrinsic tongue muscle at the chronic injured stage. These results suggest that the upper airway may be predisposed to collapse in response to bronchopulmonary C-fiber activation following chronic cervical spinal cord injury.

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Motor imagery reinforces brain compensation of reach-to-grasp movement after cervical spinal cord injury

Frontiers in Behavioral Neuroscience ◽

10.3389/fnbeh.2015.00234 ◽

2015 ◽

Vol 9 ◽

Cited By ~ 14

Author(s):

Sébastien Mateo ◽

Franck Di Rienzo ◽

Vance Bergeron ◽

Aymeric Guillot ◽

Christian Collet ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Motor Imagery ◽

Cervical Spinal Cord ◽

Cervical Spinal Cord Injury ◽

Reach To Grasp ◽

Cord Injury

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Changes in Locomotor Muscle Activity After Treadmill Training in Subjects With Incomplete Spinal Cord Injury

Journal of Neurophysiology ◽

10.1152/jn.91131.2008 ◽

2009 ◽

Vol 101 (2) ◽

pp. 969-979 ◽

Cited By ~ 57

Author(s):

Monica A. Gorassini ◽

Jonathan A. Norton ◽

Jennifer Nevett-Duchcherer ◽

Francois D. Roy ◽

Jaynie F. Yang

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Muscle Activity ◽

Muscle Activation ◽

Treadmill Training ◽

Emg Activity ◽

Incomplete Spinal Cord Injury ◽

Activation Patterns ◽

Muscle Activation Patterns ◽

Cord Injury

Intensive treadmill training after incomplete spinal cord injury can improve functional walking abilities. To determine the changes in muscle activation patterns that are associated with improvements in walking, we measured the electromyography (EMG) of leg muscles in 17 individuals with incomplete spinal cord injury during similar walking conditions both before and after training. Specific differences were observed between subjects that eventually gained functional improvements in overground walking (responders), compared with subjects where treadmill training was ineffective (nonresponders). Although both groups developed a more regular and less clonic EMG pattern on the treadmill, it was only the tibialis anterior and hamstring muscles in the responders that displayed increases in EMG activation. Likewise, only the responders demonstrated decreases in burst duration and cocontraction of proximal (hamstrings and quadriceps) muscle activity. Surprisingly, the proximal muscle activity in the responders, unlike nonresponders, was three- to fourfold greater than that in uninjured control subjects walking at similar speeds and level of body weight support, suggesting that the ability to modify muscle activation patterns after injury may predict the ability of subjects to further compensate in response to motor training. In summary, increases in the amount and decreases in the duration of EMG activity of specific muscles are associated with functional recovery of walking skills after treadmill training in subjects that are able to modify muscle activity patterns following incomplete spinal cord injury.

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Metabolic Costs and Muscle Activity Patterns During Robotic- and Therapist-Assisted Treadmill Walking in Individuals With Incomplete Spinal Cord Injury

Physical Therapy ◽

10.2522/ptj.20050266 ◽

2006 ◽

Vol 86 (11) ◽

pp. 1466-1478 ◽

Cited By ~ 194

Author(s):

Jeffrey F Israel ◽

Donielle D Campbell ◽

Jennifer H Kahn ◽

T George Hornby

Keyword(s):

Spinal Cord ◽

Muscle Activity ◽

Activity Patterns ◽

Swing Phase ◽

Emg Activity ◽

Robotic Device ◽

Incomplete Spinal Cord Injury ◽

Robotic Assisted ◽

Cord Injury ◽

Metabolic Costs

AbstractBackground and Purpose. Robotic devices that provide passive guidance and stabilization of the legs and trunk during treadmill stepping may increase the delivery of locomotor training to subjects with neurological injury. Lower-extremity guidance also may reduce voluntary muscle activity as compared with compliant assistance provided by therapists. The purpose of this study was to investigate differences in metabolic costs and lower-limb muscle activity patterns during robotic- and therapist-assisted treadmill walking. Subjects. Twelve ambulatory subjects with motor incomplete spinal cord injury participated. Methods. In 2 separate protocols, metabolic and electromyographic (EMG) data were collected during standing and stepping on a treadmill with therapist and robotic assistance. During robotic-assisted walking, subjects were asked to match the kinematic trajectories of the device and maximize their effort. During therapist-assisted walking, subjects walked on the treadmill with manual assistance provided as necessary. Results. Metabolic costs and swing-phase hip flexor EMG activity were significantly lower when subjects were asked to match the robotic device trajectories than with therapist-assisted walking. These differences were reduced when subjects were asked to maximize their effort during robotic-assisted stepping, although swing-phase plantar-flexor EMG activity was increased. In addition, during standing prior to therapist- or robotic-assisted stepping, metabolic costs were higher without stabilization from the robotic device. Discussion and Conclusion. Differences in metabolic costs and muscle activity patterns between therapist- and robotic-assisted standing and stepping illustrate the importance of minimizing passive guidance and stabilization provided during step training protocols.

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Alternate Leg Movement Amplifies Locomotor-Like Muscle Activity in Spinal Cord Injured Persons

Journal of Neurophysiology ◽

10.1152/jn.00817.2004 ◽

2005 ◽

Vol 93 (2) ◽

pp. 777-785 ◽

Cited By ~ 49

Author(s):

Noritaka Kawashima ◽

Daichi Nozaki ◽

Masaki O. Abe ◽

Masami Akai ◽

Kimitaka Nakazawa

Keyword(s):

Spinal Cord ◽

Muscle Activity ◽

Lower Limbs ◽

Emg Activity ◽

Joint Movement ◽

Experimental Conditions ◽

Biceps Femoris Muscle ◽

Cord Injury ◽

Leg Movement ◽

The Right

It is now well recognized that muscle activity can be induced even in the paralyzed lower limb muscles of persons with spinal cord injury (SCI) by imposing locomotion-like movements on both of their legs. Although the significant role of the afferent input related to hip joint movement and body load has been emphasized considerably in previous studies, the contribution of the “alternate” leg movement pattern has not been fully investigated. This study was designed to investigate to what extent the alternate leg movement influenced this “locomotor-like” muscle activity. The knee-locked leg swing movement was imposed on 10 complete SCI subjects using a gait training apparatus. The following three different experimental conditions were adopted: 1) bilateral alternate leg movement, 2) unilateral leg movement, and 3) bilateral synchronous (in-phase) leg movement. In all experimental conditions, the passive leg movement induced EMG activity in the soleus and medial head of the gastrocnemius muscles in all SCI subjects and in the biceps femoris muscle in 8 of 10 SCI subjects. On the other hand, the EMG activity was not observed in the tibialis anterior and rectus femoris muscles. The EMG level of these activated muscles, as quantified by integrating the rectified EMG activity recorded from the right leg, was significantly larger for bilateral alternate leg movement than for unilateral and bilateral synchronous movements, although the right hip and ankle joint movements were identical in all experimental conditions. In addition, the difference in the pattern of the load applied to the leg among conditions was unable to explain the enhancement of EMG activity in the bilateral alternate leg movement condition. These results suggest that the sensory information generated by alternate leg movements plays a substantial role in amplifying the induced locomotor-like muscle activity in the lower limbs.

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Intraspinal microstimulation and diaphragm activation after cervical spinal cord injury

Journal of Neurophysiology ◽

10.1152/jn.00721.2016 ◽

2017 ◽

Vol 117 (2) ◽

pp. 767-776 ◽

Cited By ~ 21

Author(s):

L. M. Mercier ◽

E. J. Gonzalez-Rothi ◽

K. A. Streeter ◽

S. S. Posgai ◽

A. S. Poirier ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Cervical Spinal Cord ◽

Emg Activity ◽

Motor Nucleus ◽

Adult Rats ◽

Intraspinal Microstimulation ◽

Emg Signal ◽

Cord Injury ◽

Diaphragm Activity

Intraspinal microstimulation (ISMS) using implanted electrodes can evoke locomotor movements after spinal cord injury (SCI) but has not been explored in the context of respiratory motor output. An advantage over epidural and direct muscle stimulation is the potential of ISMS to selectively stimulate components of the spinal respiratory network. The present study tested the hypothesis that medullary respiratory activity could be used to trigger midcervical ISMS and diaphragm motor unit activation in rats with cervical SCI. Studies were conducted after acute (hours) and subacute (5–21 days) C2 hemisection (C2Hx) injury in adult rats. Inspiratory bursting in the genioglossus (tongue) muscle was used to trigger a 250-ms train stimulus (100 Hz, 100–200 μA) to the ventral C4 spinal cord, targeting the phrenic motor nucleus. After both acute and subacute injury, genioglossus EMG activity effectively triggered ISMS and activated diaphragm motor units during the inspiratory phase. The ISMS paradigm also evoked short-term potentiation of spontaneous inspiratory activity in the previously paralyzed hemidiaphragm (i.e., bursting persisting beyond the stimulus period) in ∼70% of the C2Hx animals. We conclude that medullary inspiratory output can be used to trigger cervical ISMS and diaphragm activity after SCI. Further refinement of this method may enable “closed-loop-like” ISMS approaches to sustain ventilation after severe SCI. NEW & NOTEWORTHY We examined the feasibility of using intraspinal microstimulation (ISMS) of the cervical spinal cord to evoke diaphragm activity ipsilateral to acute and subacute hemisection of the upper cervical spinal cord of the rat. This proof-of-concept study demonstrated the efficacy of diaphragm activation, using an upper airway respiratory EMG signal to trigger ISMS at the level of the ipsilesional phrenic nucleus during acute and advanced postinjury intervals.

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Laryngeal and swallow dysregulation following acute cervical spinal cord injury

10.1101/2021.09.21.457706 ◽

2021 ◽

Author(s):

Teresa Pitts ◽

Kimberly E Iceman ◽

Alyssa Huff ◽

M Nicholas Musselwhite ◽

Michael L Frazure ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Cervical Spinal Cord ◽

Upper Airway ◽

Emg Activity ◽

Post Injury ◽

Percent Change ◽

Cord Injury ◽

Posterior Cricoarytenoid ◽

Diaphragm Activity

Proper function of the larynx is vital to airway protection, including swallow. While the swallow reflex is controlled by the brainstem, patients with cervical spinal cord injuries (cSCI) are likely at increased risk of disordered swallow (dysphagia) and pneumonia, and the underlying mechanisms are unknown. We aimed to determine if acute spinal cord injury would disrupt swallow function in animal models. We hypothesized that 1) loss of descending efferent information to the diaphragm would affect swallow and breathing differently, and that 2) loss of ascending spinal afferent information would alter central swallow regulation to change motor drive to the upper airway. We recorded amplitudes of laryngeal and inspiratory muscle electromyograms (EMGs), submental and pharyngeal muscle EMGs, and cardiorespiratory measures in freely breathing pentobarbital-anesthetized cats and rats. First, we assessed the effect of a lateral hemisection at the second cervical level (C2) in cats during breathing. Posterior cricoarytenoid (laryngeal abductor) EMG activity during inspiration increased nearly two-fold, indicating that inspiratory laryngeal drive increased following cSCI. Ipsilateral to the injury, the crural diaphragm EMG was significantly reduced during breathing (62 ± 25 percent change post-injury), but no animal had a complete termination of all activity; 75% of animals had an increase in contralateral diaphragm recruitment after cSCI, but this did not reach significance. Next, we assessed the effect of C2 lateral hemisection in cats during swallow. The thyroarytenoid (laryngeal adductor) and thyropharyngeus (pharyngeal constrictor) both increased EMG activity during swallow, indicating increased upper airway drive during swallow following cSCI. There was no change in the number of swallows stimulated per trial. We also found that diaphragm activity during swallow (schluckatmung) was bilaterally suppressed after lateral C2 hemisection, which was unexpected because this injury did not suppress contralateral diaphragm activity during breathing. Swallow-breathing coordination was also affected by cSCI, with more post-injury swallows occurring during early expiration. Finally, because we wanted to determine if the chest wall is a major source of feedback for laryngeal regulation, we performed T1 total transections in rats. As in the cat C2 lateral hemisection, a similar increase in inspiratory laryngeal activity (posterior cricoarytenoid) was the first feature noted after rat T1 complete spinal cord transection. In contrast to the cat C2 lateral hemisection, diaphragmatic respiratory drive increased after T1 transection in every rat (215 ± 63 percent change), and this effect was significant. Overall, we found that spinal cord injury alters laryngeal drive during swallow and breathing, and alters swallow-related diaphragm activity. Our results show behavior-specific effects, suggesting that swallow may be more affected than breathing is by cSCI, and emphasizing the need for additional studies on laryngeal function during breathing and swallow after spinal cord injury.

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