Spinal Cord Stimulation and Augmentative Control Strategies for Leg Movement after Spinal Paralysis in Humans

Abstract

Severe spinal cord injury is a devastating condition, tearing apart long white matter tracts and causing paralysis and disability of body functions below the lesion. But caudal to most injuries, the majority of neurons forming the distributed propriospinal system, the localized gray matter spinal interneuronal circuitry, and spinal motoneuron populations are spared. Epidural spinal cord stimulation can gain access to this neural circuitry. This review focuses on the capability of the human lumbar spinal cord to generate stereotyped motor output underlying standing and stepping, as well as full weight-bearing standing and rhythmic muscle activation during assisted treadmill stepping in paralyzed individuals in response to spinal cord stimulation. By enhancing the excitability state of the spinal circuitry, the stimulation can have an enabling effect upon otherwise "silent" translesional volitional motor control. Strategies for achieving functional movement in patients with severe injuries based on minimal translesional intentional control, task-specific proprioceptive feedback, and next-generation spinal cord stimulation systems will be reviewed. The role of spinal cord stimulation can go well beyond the immediate generation of motor output. With recently developed training paradigms, it can become a major rehabilitation approach in spinal cord injury for augmenting and steering trans- and sublesional plasticity for lasting therapeutic benefits.

Keywords: Human; Locomotion; Motor control; Neuromodulation; Neuroplasticity; Neurorehabilitation; Spinal cord injury; Spinal cord stimulation.

Conflict of interest statement

The authors declare no conflict of interest.

© 2016 John Wiley & Sons Ltd.

Figures

Figure 1

The human lumbar spinal cord circuitry can generate motor output underlying stepping and standing in response to epidural spinal cord stimulation (SCS) in the absence of task‐specific supraspinal or peripheral feedback input. (A) Top: X‐ray of the low thoracic (T) spine and an epidurally placed lead with four electrodes (white rectangles). Bottom: Sketch of a cross section through the 12th thoracic vertebra, showing the position of a dorsally placed epidural electrode (red circle) relative to the neural structures within the vertebral canal. Gray circles represent cross sections of longitudinally oriented posterior and anterior roots (sensory and motor nerve bundles, respectively) surrounding the spinal cord. (B) Generation of rhythmic activity in paralyzed legs by lumbar SCS in supine position. Surface EMG recording from unilateral quadriceps (Q), adductor (Add), hamstrings (Ham), tibialis anterior (TA), and triceps surae (TS) and inclinometer sensor trace from the induced knee movement (KM; deflection up is flexion). Subject with a chronic complete spinal cord injury, neurological level T5; stimulation parameters: 30 Hz, 9 V. Modified with permission from 21. (C) Generation of motor output underlying standing in paralyzed legs by lumbar SCS. Stimulation at 10 and 16 Hz induced leg extension from an initially flexed position, with “sustained” EMG pattern and stereotyped amplitude modulation. Increasing the SCS frequency (21, 31 Hz) changed the EMG pattern from sustained to rhythmic. KM, knee movement derived from goniometric data. Stick figures are constructed based on the knee angle data, with the lower legs manually supported in a horizontal position. Subject with a chronic complete spinal cord injury, neurological level T7; stimulation intensity: 10 V in all cases. Modified with permission from 58.

Figure 2

Epidural lumbar spinal cord stimulation (SCS) can generate extensive rhythmic lower limb activity during assisted treadmill stepping and induce full weight‐bearing standing. (A) Lower limb EMG activity induced by therapist‐assisted, partially (50%) body weight‐supported treadmill stepping (0.36 m/s) without (left) and with epidural lumbar SCS. Adding SCS at 30 Hz and supra‐threshold intensity considerably augmented the rhythmic EMG activity and recruited muscles that had not responded to proprioceptive feedback input produced during stepping alone. Leg movements were continuously assisted by therapists. EMG recordings from unilateral quadriceps (Q), hamstrings (Ham), tibialis anterior (TA), and triceps surae (TS); black horizontal bars mark stance phases. Subject with a chronic complete spinal cord injury, neurological level C7. Modified with permission from 9. (B) Kinematic representation of sitting to standing transition induced by epidural SCS applied at 15 Hz and supra‐threshold intensity. After intensive training, the subject could start and maintain full weight‐bearing standing under SCS, with minimal self‐assistance for balance. Subject with a chronic motor‐complete, sensory‐incomplete spinal cord injury, neurological level T2. Modified with permission from 75.

Figure 3

Strategies to control motor output generated by SCS below a paralyzing spinal cord injury. (A) Proprioceptive feedback as a source of control. Lower limb EMG activity of quadriceps (Q), hamstrings (Ham), tibialis anterior (TA), and triceps surae (TS) induced by continuous 30‐Hz SCS during therapist‐assisted standing and treadmill stepping (0.36 m/s) with body weight support (50%). The addition of step‐specific sensory feedback changed continuous EMG patterns to rhythmic ones, and nonresponding muscles in standing responded with rhythmic activity during stepping. Rhythmic activity immediately stopped as soon as the treadmill belt was stopped, despite ongoing stimulation. Same subject as in Fig. 2A. (B) Minimal translesional descending input as a source of control. Kinematic representation of the paralyzed leg when the subject in supine position actively attempted to perform a hip‐flexion movement during ongoing 30‐Hz SCS. Same subject as in Fig. 2B. Modified with permission from 75. (C) SCS frequency entrains the motoneuron pool firing rate and may be used to control the muscle force produced. Continuous sequences of rhythmic EMG activity produced by SCS at 21 Hz and 31 Hz (cf. Fig. 1C) along with detailed EMG data extracted from the time window highlighted by the dashed boxes. Increased numbers of responses per burst were shown to produce increased levels of muscle force in rat 68. (D) Segmental‐selective muscle recruitment by SCS. Stimulus‐triggered EMG responses of the L2–L4 innervated Q and the L5–S2 innervated TS to 2‐Hz stimulation and incremental intensities. Stimulation from the rostral site (12th thoracic vertebra) allowed relatively selective recruitment of upper lumbar posterior roots, stimulation from the caudal site (1st lumbar vertebra) recruited lower lumbar/upper sacral posterior roots at lower intensities. Red diamonds indicate vertebral positions of the active cathode. Left: subject with complete spinal cord injury at C5; right: subject with a motor‐complete, sensory‐incomplete injury at T10. Modified with permission from 62.