Intraspinal microstimulation preferentially recruits fatigue-resistant muscle fibres and generates gradual force in rat.

Intraspinal microstimulation (ISMS), a novel rehabilitative therapy consisting of stimulation through fine, hair-like microwires targeted at the ventral spinal cord, has been proposed for restoring standing and walking following spinal cord injury. This study compared muscle recruitment characteristics of ISMS with those produced by peripheral nerve cuff stimulation (NCS). Thirty-three minutes of either ISMS or NCS at 1, 20 or 50 s(-1) and 1.2 x threshold (T) amplitude depleted glycogen from muscle fibres of vastus lateralis and rectus femoris. ISMS and NCS were also carried out at 20 s(-1) and 3.0T. Muscle serial sections were stained for glycogen and for myosin heavy chain (MHC)-based fibre types using a panel of monoclonal antibodies. The results of this study show that ISMS recruited fatigue-resistant (FR) fibres at 2.9, 1.9, 1.7 and 2.5 times their relative MHC content at 1, 20 and 50 s(-1) 1.2T and 20 s(-1) 3.0T, respectively. In contrast, NCS recruited FR fibres at 1.2, 1.0, 2.1 and 0.0 times their MHC content at 1, 20 and 50 s(-1) 1.2T and 20 s(-1) 3.0T, respectively. The proportion of FR fibres recruited by ISMS and NCS was significantly different in the 20 s(-1) 3.0T condition (P < 0.0001). We also report that force recruitment curves were 4.9-fold less steep (P < 0.019) for ISMS than NCS. The findings of this study provide evidence for the efficacy of ISMS and further our understanding of muscle recruitment properties of this novel rehabilitative therapy.

The role of neuromuscular properties in determining the end-point of a movement.

How does the activation of several muscles combine to produce reliable multijoint movements? To study this question, we stimulated up to six sites in muscles, nerves, and the spinal cord. Flexion and extension of the hip, knee, and ankle were elicited in anesthetized and decerebrate cats. The movements occurred largely in the sagittal plane against a constant spring load and covered most of the passive range of motion of the cat's limb. The movements of the end-point (foot) were compared with predictions based on vectorial summation of end-point movements elicited by stimulating single electrodes. The lengths of the movements produced by stimulating more than one site exceeded what was expected from linear summation for small movements (<3 cm) and showed a less than linear summation for large movements (>11 cm). The data were compared with muscle and limb models. Since the deviations from linearity were predictable as a function of distance, adjustments might easily be learned by trial and error. The summation was less complete for spinal stimulation, compared to nerve and muscle stimulation, so spinal circuits do not appear to compensate for the nonlinearities. Movements were elicited from positions of the limb not only in a neutral position, but also in front and behind the neutral position. A degree of convergence was seen, even with stimulation of some individual muscles, but the convergence increased as more muscles were stimulated and more joints were actively involved. This suggests that convergence to an equilibrium-point arises at least partly from muscle properties. In conclusion, there are deviations from linear vectorial summation, and these deviations increase when more muscles are stimulated. The convergence to an equilibrium-point may simplify the computations needed to produce movements involving many muscles.

Limb movements generated by stimulating muscle, nerve and spinal cord.

We have compared the movements generated by stimulation of muscle, nerve, spinal roots and spinal cord in anesthetized, decerebrate and spinalized cats. Each method produced a full range of movements of the cat's hind limb in the sagittal plane against a spring load, except for stimulation of the roots. Stimulation of the dorsal roots produced movements that were mainly up and forward, whereas stimulation of the ventral roots produced complementary movements (down and backward). Results from stimulation in the intermediate areas of the spinal cord were compared to predictions of the "movement primitives" hypothesis. We could not confirm that the directions were independent of stimulus amplitude or the state of descending inputs. Pros and cons of stimulating at some sites were provisionally considered for the reliable control of limb movements with functional electrical stimulation (FES) in clinical conditions.

Selective activation of muscle groups in the feline hindlimb through electrical microstimulation of the ventral lumbo-sacral spinal cord.

Selective activation of muscle groups in the feline hindlimb by electrical stimulation of the ventral lumbo-sacral spinal cord was investigated. Spinal cord segments L5 to S1 were mapped using a penetrating tungsten needle electrode. Locations that produced isolated contraction of quadriceps, tibialis anterior or triceps surae/plantaris muscles when stimulated with a current of 40 microA or less, and in which spread of activity to other muscles was not detected after increasing the stimulus to at least twice the threshold level, were defined as belonging to the target muscle's "activation pool." The quadriceps activation pool was found to extend from the beginning of L5 to the middle of L6. The tibialis anterior activation pool extended from the beginning of L6 to the middle of L7, and the triceps surae/plantaris activation pool extended from the caudal end of L6 to the beginning of S1. The three activation pools were located in Rexed motor lamina IX and their spatial organization was found to correspond well with that of the anatomically defined motor pools innervating the same muscles. The spatial and functional segregation of motor pools manifested at the spinal cord level can have direct applications in the areas of functional electrical stimulation and motor control.

Muscle recruitment through electrical stimulation of the lumbo-sacral spinal cord.

The goal of this study was to determine the feasibility of producing graded muscle contraction in individual muscles or muscle groups by electrically stimulating motor neurons in the lumbo-sacral spinal cord. Recruitment curves were obtained for quadriceps, tibialis anterior and triceps surae/plantaris by stimulating their activation pools in the ventral horn of the feline spinal cord. Mean twitch times-to-peak for quadriceps, tibialis anterior and triceps surae/plantaris were 33.0, 41.0, and 36.0 ms, respectively. Twitch duration as a function of stimulus strength demonstrated a mixed motor unit recruitment order, distinctively different from the inverse recruitment order exhibited by conventional methods of electrical stimulation of peripheral nerve. The recruitment curve slopes (expressed as a percentage of maximum force per nanocurrent of delivered charge) were shallow: 7.9 for quadriceps, 2.6 for tibialis anterior and 8.5 for triceps surae/plantaris. These results show that graded control of force in individual muscles or muscle groups can be obtained through spinal cord stimulation, and suggest that spinal cord stimulation could be used for functional neuromuscular stimulation applications.

Proposed specifications for a lumbar spinal cord electrode array for control of lower extremities in paraplegia.

The goal of the study was to provide specifications for a stimulating electrode array to be implanted in the lumbosacral spinal cord as part of a functional neuromuscular stimulation (FNS) system for control of lower extremity muscles in paralyzed individuals. Dual channel stimulation of the quadriceps activation pool in the feline ventral lumbo-sacral spinal cord was performed to measure electrode interactions and to explore the effect of various stimulation paradigms on muscle fatigue. There was no measurable overlap in the populations of motor neurons activated from two different electrodes for spacings > or = 1 mm with currents below 100 microA. However, a statistically significant increase in the population of activated fibers due to current summation was observed when stimuli > or = 70 microA were simultaneously presented through pairs of electrodes within 3 mm of each other. Fatigue effects were studied with three paradigms: 1) stimuli were delivered through a single electrode, 2) stimuli were delivered through two electrodes with the stimulus to the second electrode presented during the refractory period of fibers stimulated by the first electrode, and 3) stimuli were interleaved between the two electrodes such that the stimulus to one electrode was presented midway between stimuli to the other electrode, and the rate of stimulation through a single electrode was half that used in the first two paradigms. Dual channel refractory and single channel stimulation did not differ from each other in the rate at which the muscle fatigued, in both cases the force decayed to 30% of its initial level within 2 min of the initiation of the stimulation regime, whereas the force with interleaved stimulation was still above the initial force at this time due to strong potentiation. Based on these results and on and activation pool dimensions obtained in an earlier study, preliminary specifications are presented for an electrode array to be implanted in the human spinal cord for functional neuromuscular stimulation.