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Getting the Spinal Cord to Think for Itself

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Getting the Spinal Cord to Think for Itself NEUROLOGICAL REVIEW SECTION EDITOR: DAVID E. PLEASURE, MD Getting the Spinal Cord to Think for Itself Robert G. Kalb, MD espite the interruption in communication between the brain and lower centers by spi- nal cord injury, many of the neurons engaged in generating locomotion survive. Sev- eral strategies have been used to activate spinal cord circuitry independent of the higher centers, including direct electrical stimulation, pharmacological agents, and training Dprograms that involve moving the legs through the motions of walking. Ambulatory leg movements are achieved by these interventions, leading to substantial functional improvements in the subset of patients with incomplete spinal cord injury. The neurobiological basis for these phenomena likely in- volves activity-dependent reconfiguration of synaptic connections within the spinal cord. Fostering this process may lead to further benefits for individuals with spinal cord injury. Arch Neurol. 2003;60:805-808 Within the realm of mindless activities, ing walking. The following 2 features bear only breathing rivals walking. Conscious highlighting: (1) even when discon- control can be superimposed, but munch- nected from supraspinal inputs, the iso- ing on a muffin and glancing at a news- lated spinal CPG can generate ambula- paper while walking is routine. Compen- tory alternating leg movements, and (2) satory minor adjustments for surface the isolated CPG circuitry can be trained irregularities, balance, speed, and rhythm to learn specific tasks. These 2 key prop- essentially proceed by autopilot. The neu- erties have captured the imagination of re- roanatomical system that subserves this re- searchers in the spinal cord injury (SCI) markable ability is widely distributed, in- field. If the neuronal ensemble within lum- volving neurons in the cerebral cortex, bar enlargement can be stimulated to gen- brainstem, cerebellum, and spinal cord. erate ambulatory leg movements, could Perhaps because of its presence in even the this form the basis for walking by indi- most primitive of chordates, the spinal cord viduals with SCI? Evidence now exists that is often thought to receive instructions pas- this approach can lead to important func- sively from higher centers. A consortium tional benefits for individuals with SCI. of neurons within the upper lumbar cord To begin to determine the utility of termed the central pattern generator (CPG) various methods for stimulating the spi- plays a fundamental role by interpreting nal CPG, it is important to identify and descending and segmental afferent sig- quantify the deficits that exist in individu- nals and patterning the firing of motor neu- als with clinically incomplete SCI.2 The rons.1 This network of neurons drives the characteristic abnormalities seen on gait rhythmic activation and relaxation of evaluation of individuals with SCI in- groups of leg muscles and coordinates the clude a reduction in walking speed, a movement of one leg with the other. longer swing-stance cycle duration, and a Studies of laboratory animals and, to shorter stride length. Angular displace- a lesser extent, human beings have pro- ments of leg joints during walking devi- vided insight into the structure and func- ate substantially from those seen in healthy tion of the spinal cord circuitry underly- individuals. Specific therapeutic interven- tions may lead to amelioration of particu- From the Department of Neurology, The Children’s Hospital of Philadelphia, lar walking deficits. It seems likely that if Philadelphia, Pa. a series of small improvements in these (REPRINTED) ARCH NEUROL / VOL 60, JUNE 2003 WWW.ARCHNEUROL.COM 805 ©2003 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 proved to be more difficult, if not impossible, to achieve. Medications Used to Alleviate Spasticity Second, although visible leg movements were observed (and could be recorded by means of surface electromy- Central actions ography), they were feeble. It is questionable whether elec- Glycinergic Glycine trically stimulating the spinal cord engenders sufficient Threonine leg strength to permit weight bearing and walking. De- Noradrenergic spite these limitations, the demonstration of a human lum- Tizanidine hydrochloride bar spinal cord CPG is important. The generation of in- Clonidine hydrochloride choate walking movements in individuals with complete Chlorpromazine hydrochloride SCI has significant implications, as will be described Propranolol hydrochloride Serotonergic herein. Cyproheptidine hydrochloride An alternative electrical stimulation approach has GABAergic been used in individuals with incomplete SCI. Func- Diazepam tional electrical stimulation (FES) involves direct stimu- Progabide lation of peripheral nerves and/or muscles, in an at- Baclofen tempt to augment motor abilities that were curtailed by Other the initial injury.4-6 Some devices simply stimulate leg flex- Morphine sulfate Peripheral actions ors when a hand switch is pressed and stimulate leg ex- Dantrolene sodium tensors when released. More sophisticated multichan- Botulinum toxin nel devices with tilt sensors providing feedback are also Anesthetics available. Mastery of the FES-assisted ambulation re- Benzocaine quires a prolonged training period under the attentive Lidocaine hydrochloride (Xylocaine) guidance of a skilled therapist. In a multicenter Cana- dian study,4 application of FES to individuals with in- Abbreviation: GABAergic, secreting ␥-aminobutyric acid. complete SCI led to significant improvement of walking speed, stride length, and cycle duration. The effects on measures can be achieved, the aggregate benefit will walking could be attributed to the FES and training per lead to the most important outcome, an improvement se. Improvement in gait was seen in all individuals, re- in function. gardless of the severity of the initial deficit. The relative Several methods have been used to stimulate the iso- importance of FES vs training varied as a function of the lated human lumbar spinal cord and have met with vari- initial deficit. Individuals who began this program with able success in eliciting walking. Beyond the intrinsic ef- the smallest deficits experienced the most improve- ficacy of individual stimulation paradigms, a number of ment, and the increase in walking speed was entirely at- other factors have an impact on the utility of these ap- tributable to the training, not FES. proaches, including the age of the patient, the interval It has long been recognized that spasticity can be a between injury and stimulation, and the severity of the significant impediment to walking for individuals with SCI. The major approaches tried include (1) direct elec- SCI. The pharmacotherapeutic mainstays for individu- trical stimulation of the lumbar spinal cord, peripheral als with SCI include the antispasticity medications such nerves, or muscles; (2) pharmacological activation of spe- as ␥-aminobutyric acid, serotonin receptor antagonists, cific subtypes of neurotransmitter receptors; and (3) ac- and ␣-adrenergic receptor agonists (a complete list of tivation of segmental afferent nerve fibers in the leg by antispasticity medications is given in the Table).7,8 On moving paralyzed limbs through the trajectory of nor- the other hand, some degree of increased leg tone is help- mal walking. ful for these individuals by enabling upright posture and In the intact nervous system, descending inputs from promoting walking. Increasing antispasticity medica- brainstem neurons from the pedunculopontine nucleus tions past a threshold dose leads to worsening of gait in and the mesencephalic locomotor region provide a tonic ambulatory individuals with SCI. Titration of therapy with drive to the spinal CPG that is needed for locomotion. these drugs to achieve an optimal level of reflex tone in In an attempt to mimic this input, epidural stimulation legs must be tailored to meet individual needs. at the T10 through L1 vertebral levels was provided to More recent attention has turned to the idea that selected individuals with a complete SCI.3 One of the jus- some of the drugs used to control spasticity might be ca- tifications for this invasive approach is that epidural spi- pable of triggering or facilitating patterned leg move- nal cord stimulation is an accepted means of reducing ments. Studies of laboratory animals indicate this ap- spasticity. Epidural stimulation led to steplike move- proach could be very promising. For example, when the ␣ ments of the leg with organized flexion/extension of mul- 2-noradrenergic agonist clonidine hydrochloride is tiple groups of muscles. By changing stimulation vari- administered to cats with an acute spinal cord transec- ables, such as the strength of the electrical input and the tion, normal-appearing walking and hind-limb weight frequency and location along the dorsal spinal cord, in- support can be elicited.9 In addition, when animals vestigators were able to convert tonic leg extension into with chronic SCI are trained to walk, the administra- rhythmic and well-coordinated steplike movements. Al- tion of clonidine had significant additive effects that though this work is a remarkable achievement, there are increased the maximum speed of walking.10 Even un- some caveats. First, although steplike movements could trained cats with chronic SCI benefited from clonidine be elicited in a single leg, alternating leg movements administration. (REPRINTED) ARCH NEUROL / VOL 60, JUNE 2003 WWW.ARCHNEUROL.COM 806 ©2003 American
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