Motor control in the human spinal cord and the repair of cord function.

In this review we describe clinical and neurophysiological features of motor control in human spinal cord injury based on two models. First, motor control is considered in subjects with injury-induced complete division of the spinal cord from brain and brainstem structures, and second, in those in which the division is partial. We describe motor control in terms of segmental and plurisegmental reflex activity that dominates motor unit output to the muscles following complete separation from the brain motor structures by accidental injury. With incomplete separation of the spinal cord from brain structures, motor control is defined as the voluntary manipulation of reflex and automatic activity integrated with internal and external feedback signals. We review here motor control found after complete spinal cord injury with paradigm of single and regular-repeating stimuli applied to elicit cutaneous and muscle stretch reflex responses. We argue, that isolated spinal cord neural circuitry is capable of organizing characteristic reflex events that depend on the characteristics of the stimulus. Also, the profile of residual brain and brainstem, modified by the reduction in descending long spinal tract fibers arriving at their targets in the spinal gray matter, produces characteristic changes in motor output to the muscles that leads to the development of new neural strategies for control of segmental and plurisegmental neural circuitry. In the second part of this review, we discuss available treatment modalities for impaired cord function and briefly outline neurobiological interventions under development for repair of spinal cord injury.

Functional magnetic resonance imaging of the human motor cortex before and after whole-hand afferent electrical stimulation.

Electrical stimulation of the whole hand using a mesh-glove has been shown to improve volitional movement of the hand and arm, and decrease muscle hypertonia after hemispherical stroke in patients who have reached a recovery plateau. The goal of this study was to investigate the effect of stimulation of the nerve afferents of the hand on brain cortical activity elicited by whole-hand subthreshold stimulation for sensation in humans with intact nervous systems. Brain cortical activity in 6 healthy subjects (30-45 years) was studied using blood oxygenation level-dependent functional Magnetic Resonance Imaging during a test motor task, finger-to-thumb tapping and after 20 minutes of mesh-glove stimulation of the resting hand prior to performance of an identical motor task, to test the changes in the conditioned motor task established after 20 minutes of mesh-glove stimulation. Fifteen contiguous echo-planar sequences parallel to the bicommissural plane were acquired for functional magnetic resonance. Post-processing of image data included correction of motion artefacts and calculation of correlation coefficients between the signal intensity of pixels during rest and finger tapping and a rectangular reference wave function. The functional Magnetic Resonance Imaging examinations revealed a signal increase in the primary and secondary motor and somatosensory areas when comparing the number of activated pixels during test and conditioned motor tasks. Our preliminary study indicated that change occurred in a definite pattern in the region of the regional cerebral blood flow of the brain cortex after mesh-glove whole-hand stimulation at the subthreshold level for sensation. We assumed that this increase in regional cerebral blood flow also reflected augmented neuronal activity.

Omental transposition in chronic spinal cord injury.

The results of omental transposition in chronic spinal cord injury have been reported in 160 patients operated upon in the United States, Great Britain, China, Japan, India and Mexico, with detailed outcomes reported in few studies. Recovery of function to a greater degree than expected by natural history has been reported. In this series, 15 patients with chronic traumatic spinal cord injury (> 1.5 years from injury) underwent transposition of pedicled omentum to the area of the spinal cord injury. Of the first series of four patients who were operated upon in 1988, one died, one was lost to follow-up and two were followed with sequential neurological examinations and Magnetic Resonance Imaging (MRI) scans preoperatively, at 1 year post injury and 4 1/2 years post injury. Another 11 patients were operated in 1992 and underwent detailed neurological and neurophysiological examinations and had MRI scans preoperatively and every 4 months for at least 1 year after surgery. All patients completed a detailed self-report form. Of the total of 13 operated patients in both series followed for 1-4 1/2 years, six reported some enhanced function at 1 year and five of these felt the changes justified surgery primarily because of improved truncal control and decreased spasticity. MRI scans showed enlargement of the spinal cord as compared to preoperative scans in seven patients. Increased T2 signal intensity of the spinal cord was found by 1 year after surgery in eight of 13 operated patients. Neurophysiological examinations of 11 patients in the second series agreed with self-reports of increases or decreases in spasticity (r = 0.65, P < 0.03). Somatosensory evoked potentials and motor evoked potentials at 4 month intervals up to 1 year in these patients showed no change after surgery. Neurological testing, using the American Spinal Injury Association (ASIA) and International Medical Society of Paraplegia (IMSOP) international scoring standards, failed to show any significant changes when the 1-year post operative examination was compared to the first preoperative examination except for decreased sensory function after surgery which approached statistical significance. When the 11 patients in the second series were compared to eight non-operated matched patients, followed for a similar length of time, no significant differences were found. Complications encountered in the operated patients from both series included one postoperative death from a pulmonary embolus, one postoperative pneumonia, three chronic subcutaneous cerebrospinal fluid (CSF) fistulae requiring wound revision, and one patient who developed biceps and wrist extensor weakness bilaterally requiring graft removal. We conclude that the omental graft remains viable over time and this operation can induce anatomical changes in the spinal cord as judged by MRI. Some patients reported subjective improvement but this was not supported by objective testing. We, therefore, find no justification for further clinical trials of this procedure in patients who have complete or sensory incomplete lesions. Further testing in motor incomplete patients would seem appropriate only with compelling supportive data.

Modification of motor control of wrist extension by mesh-glove electrical afferent stimulation in stroke patients.

OBJECTIVE: To study the effect of mesh-glove afferent stimulation on motor control of voluntary wrist movement in stroke patients who have chronic neurological deficits. DESIGN: Case series. Motor control was evaluated by surface EMG of the arm muscles and kinematics of voluntary wrist movements on 3 occasions: before and immediately after the initial session of mesh-glove stimulation, and then after a daily mesh-glove stimulation program conducted over several months. SETTING: Tertiary care center. PATIENTS: The inclusion criteria were: a history of stroke lasting longer than 6 months; completion of a rehabilitation program during early recovery; and preserved cognitive and communicative ability. Fourteen referred patients (age 63 +/- 9yr; time since stroke 31 +/- 22mo) fulfilled the criteria and completed the daily stimulation program. INTERVENTION: A single initial and then daily mesh-glove electrical afferent stimulation was applied to the hand of the involved upper limb for 20 to 30min. MAIN OUTCOME MEASURES: Surface EMGs from the affected biceps brachii and wrist extensor muscles and amplitudes of wrist movements were analyzed. RESULTS: The single, initial mesh-glove application had no effect on outcome measures. Following a daily mesh-glove stimulation program, however, both the amplitude of wrist extension movement and wrist extensor integrated EMG were significantly increased while coactivation of biceps brachii decreased. These findings were most prominent in subjects with partially preserved voluntary wrist movements. CONCLUSION: We conclude that daily mesh-glove stimulation can modify altered motor control and improve voluntary wrist extension movement in stroke subjects with chronic neurological deficits.

Mesh-glove. 1. A method for whole-hand electrical stimulation in upper motor neuron dysfunction.

A newly devised method for electrical stimulation via a wired mesh-glove is described. The stimulation paradigm is novel in that a whole hand is the target of stimulation. Specific standardized stimulation modalities are reviewed. The protocol for mesh-glove stimulation for patients with and without volitional movements, but increased muscle tone is outlined. A sequenced program based on restoration of motor functions is described. The mesh-glove stimulation is well suited for home use. On the basis of our experience working with 40 patients after stroke, head and spinal cord injuries, we concluded that this procedure is beneficial and safe.

Mesh-glove. 2. Modulation of residual upper limb motor control after stroke with whole-hand electric stimulation.

The effects of whole-hand electrical stimulation via a wired mesh-glove upon the residual motor control of the upper extremity are described. Clinical observations were made in 2 patients with nonfunctional upper limbs, 4 and 2 years after stroke, who had been enrolled in the home mesh-glove program for 6 and 4 months, respectively. The stimulation paradigm is novel and the target of stimulation is the hand. Preliminary results indicate beneficial effects such as reduction in muscle hypertonia and facilitation of isolated hand movements.

Spinal cord stimulation for the control of spasticity in patients with chronic spinal cord injury: I. Clinical observations.

The effectiveness of spinal cord stimulation for control of spasticity was studied in 59 spinal cord injury patients. SCS was markedly or moderately effective in reducing spasticity in 63% of the patients. We found that control of spasticity by SCS was not correlated with the severity of spasticity, the type of spasticity (flexor or extensor), or the ability to ambulate. However, stimulation was more effective in patients with incomplete cervical lesions than in complete cervical lesions. Stimulation below the lesion was more effective than above. We conclude that SCS was effective when electrodes were properly positioned below the lesion over the posterior aspect of the spinal cord in patients with some residual spinal cord function. We hypothesize that SCS controls spasticity by modification of activity of spinal-brainstem-spinal loops and by suppression of segmental excitation through antidromic activation of propriospinal pathways.

Suprasegmentally induced motor unit activity in paralyzed muscles of patients with established spinal cord injury.

In an attempt to demonstrate the presence of functional descending fibers in patients with clinically apparent functional spinal cord transection, we examined electromyographically recorded paralyzed leg muscle responses to the Jendrassik and other reinforcement maneuvers. Two patterns were observed: a low-amplitude, short onset time reinforcement maneuver response (RMR) restricted to one to three muscle groups (RMR1), and a larger-amplitude response with a longer onset time that occurred bilaterally in essentially all of the recorded muscles (RMR2). The responses imply preserved descending facilitory influence on isolated populations of motor units (RMR1) or on segmental interneuron pools (RMR2). Such findings indicate the presence of functioning fibers traversing the injured portion of the spinal cord in patients diagnosed as having a complete lesion. In such cases, it is possible for patients to initiate subclinical motor unit activity or suprasegmentally induced gross movement through reinforcement maneuvers, but not to control the amplitude or duration of the response.

Neurocontrol of upper motor neurone muscle paralysis.

An attempt was made to describe upper motor neurone dysfunctions on the basis of changes in volitional activity, the effects of reinforcement maneuvers on motor units and sustained and unsustained characteristics of segmental reflexes. According to the above criteria, patients with paralysis due to established spinal cord injury can be divided into groups with clinical and subclinical paralysis, clinical paralysis with subclinical evidence of residual suprasegmental motor control, and clinically incomplete paralysis with a subclinical variety of neurocontrol patterns of motor activities. This categorization of paralysis according to neurocontrol criteria is opening new avenues to the use of residual motor activity for the modification of abnormal motor control by peripheral nerve stimulation and spinal cord stimulation procedures for the alteration of upper motor neurone dysfunctions.

Remarks on spinal cord stimulation and the placebo effect.

Spinal cord stimulation, which has been shown to be beneficial in multiple sclerosis as well as in sustained spinal cord injury, works through modification of specific motor mechanisms. This modification occurs through regional recruitment of spinal cord activity in posterior aspects of the spinal cord. Substantial involvement of the placebo effect can be ruled out by noting the persistence of beneficial effects observed in spinal cord injury patients and by the fact that the effects are related only to depolarization of posterior structures of the spinal cord, rather than to perception of a 'tingling' sensation caused by spinal cord stimulation. Such a sensation can also occur when electrodes are over anterior or lateral structures of the spinal cord, when the stimulation is not effective in alleviating motor symptoms.

Clinical evaluation of the effect of spinal cord stimulation on motor performance in patients with upper motor neuron lesions.

The effect of chronic electrical stimulation of the spinal cord was evaluated in a group of 24 patients with multiple sclerosis, spinal cord injury, and degenerative disorders of the central nervous system. The systems for stimulation had been implanted from 12 to 30 months prior to completion of evaluation. At the time of completion of evaluation, 23 of the 24 patients still had implanted systems, although 6 of them had not used spinal cord stimulation because of no noticeable effect. In 3 patients stimulation had been disconnected because of technical failure of the system. In 1 patient the system had been removed 8 weeks after implantation because of inflammation in the under-skin receiver pocket. The effects on motor performance of the remaining 14 patients who had continuously active systems were improved bladder control, diminished spasticity, improved movement coordination, and increased endurance.

Neurophysiological evaluation of chronic spinal cord stimulation in patients with upper motor neuron disorders.

Spinal cord stimulation was found to be an effective method for improving motor performance in patients with upper motor neuron disorders. Electromyographic analysis of segmental and suprasegmental activity was performed in 11 patients who had used spinal cord stimulation for more than 12 months. Neurophysiological analysis of electromyographic findings revealed improvement of volitional motor control and a reduction of spasticity in the examined muscles of the lower limbs in all patients.