Matthew C. Tresch

The construction of movement by the spinal cord

We used a computational analysis to identify the basic elements with which the vertebrate spinal cord constructs one complex behavior. This analysis extracted a small set of muscle synergies from the range of muscle activations generated by cutaneous stimulation of the frog hindlimb. The flexible combination of these synergies was able to account for the large number of different motor patterns produced by different animals. These results therefore demonstrate one strategy used by the vertebrate nervous system to produce movement in a computationally simple manner.

The case for and against muscle synergies

A long standing goal in motor control is to determine the fundamental output controlled by the CNS: does the CNS control the activation of individual motor units, individual muscles, groups of muscles, kinematic or dynamic features of movement, or does it simply care about accomplishing a task? Of course, the output controlled by the CNS might not be exclusive but instead multiple outputs might be controlled in parallel or hierarchically. In this review we examine one particular hypothesized level of control: that the CNS produces movement through the flexible combination of groups of muscles, or muscle synergies. Several recent studies have examined this hypothesis, providing evidence both in support and in opposition to it. We discuss these results and the current state of the muscle synergy hypothesis.

Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors

Previous studies have suggested that the motor system may simplify control by combining a small number of muscle synergies represented as activation profiles across a set of muscles. The role of sensory feedback in the activation and organization of synergies has remained an open question. Here, we assess to what extent the motor system relies on centrally organized synergies activated by spinal and/or supraspinal commands to generate motor outputs by analyzing electromyographic (EMG) signals collected from 13 hindlimb muscles of the bullfrog during swimming and jumping, before and after deafferentation. We first established that, for both behaviors, the intact and deafferented data sets possess low and similar dimensionalities. Subsequently, we used a novel reformulation of the non-negative matrix factorization algorithm to simultaneously search for synergies shared by, and synergies specific to, the intact and deafferented data sets. Most muscle synergies were identified as shared synergies, suggesting that EMGs of locomotor behaviors are generated primarily by centrally organized synergies. Both the amplitude and temporal patterns of the activation coefficients of most shared synergies, however, were altered by deafferentation, suggesting that sensory inflow modulates activation of those centrally organized synergies. For most synergies, effects of deafferentation on the activation coefficients were not consistent across frogs, indicating substantial interanimal variability of feedback actions. We speculate that sensory feedback might adapt recruitment of muscle synergies to behavioral constraints, and the few synergies specific to the intact or deafferented states might represent afferent-specific modules or feedback reorganization of spinal neuronal networks.

Motor coordination without action potentials in the mammalian spinal cord.

Coordination of neuronal activity to produce movement is generally thought to depend on spike activity in premotor interneuronal networks. Here we show that even without such activity, the neonatal rat spinal cord could produce a stable motor rhythm mediated by the synchronization of motor neuron oscillations across gap junctions. These rhythms, however, were not coordinated between motor pools in different parts of the spinal cord. We further showed that neural coordination through gap junctions contributed to the fundamental organization and function of spinal motor systems. These results suggest that neural coordination across gap junctions is important in motor-pattern generation in the mammalian spinal cord.

Double dissociation of spatial and object visual memory: evidence from selective interference in intact human subjects

A functional dissociation of the spatial and object visual systems was produced by selective interference in intact young adults. Subjects were instructed to remember the location of a dot in a spatial memory test, and the form of an object memory test. As predicted by current notions of dissociable visual systems in the primate, spatial memory was selectively impaired by a movement discrimination spatial task, whereas object memory was selectively impaired by a color discrimination object task.

Responses to spinal microstimulation in the chronically spinalized rat and their relationship to spinal systems activated by low threshold cutaneous stimulation

Abstract We describe the responses evoked by microstimulation of interneuronal regions of the spinal cord in unanesthetized rats chronically spinalized at T10–T12. One to three weeks after spinalization, sites in the lumbar spinal cord were stimulated using trains of low current microstimulation. The isometric force produced by stimulation of a spinal site was measured at the ankle. Responses were reliably observed from stimulation of a region within the first 1250 µm from the dorsal surface of the spinal cord. These responses were clearly not due to direct motoneuronal activation and were maintained after chronic deafferentation. The force evoked by microstimulation and measured at the ankle varied smoothly across the workspace. Simultaneous stimulation of two sites in the spinal cord produced a response that was a simple linear summation of the responses evoked from each of the sites alone. Microstimulation generally produced a highly non-uniform distribution of response directions, biased toward responses which pulled the limb toward the body. Within these distributions there appeared to be two main types of responses. These different types of responses were preferentially evoked by microstimulation of different rostrocaudal regions of the spinal cord. This anatomical organization paralleled the spinal cutaneous somatotopy, as assessed by recording cutaneous receptive fields of neurons at sites to which the microstimulation was applied. This relationship was maintained after chronic deafferentation. The findings described here in the rat spinal cord in large part replicate those previously described in the frog.

Contributions of intrinsic motor neuron properties to the production of rhythmic motor output in the mammalian spinal cord

Motor neurons are endowed with intrinsic and conditional membrane properties that may shape the final motor output. In the first half of this paper we present data on the contribution of I(h), a hyperpolarization-activated inward cation current, to phase-transition in motor neurons during rhythmic firing. Motor neurons were recorded intracellularly during locomotion induced with a mixture of N-methyl-D-aspartate (NMDA) and serotonin, after pharmacological blockade of I(h). I(h) was then replaced by using dynamic clamp, a computer program that allows artificial conductances to be inserted into real neurons. I(h) was simulated with biophysical parameters determined in voltage clamp experiments. The data showed that electronic replacement of the native I(h) caused a depolarization of the average membrane potential, a phase-advance of the locomotor drive potential, and increased motor neuron spiking. Introducing an artificial leak conductance could mimic all of these effects. The observed effects on phase-advance and firing, therefore, seem to be secondary to the tonic depolarization; i.e., I(h) acts as a tonic leak conductance during locomotion. In the second half of this paper we discuss recent data showing that the neonatal rat spinal cord can produce a stable motor rhythm in the absence of spike activity in premotor interneuronal networks. These coordinated motor neuron oscillations are dependent on NMDA-evoked pacemaker properties, which are synchronized across gap junctions. We discuss the functional relevance for such coordinated oscillations in immature and mature spinal motor systems.

Coordination and localization in spinal motor systems.

We review here experiments examining the hypothesis that vertebrate spinal motor systems produce movement through the flexible combination of a small number of units of motor output. Using a variety of preparations and techniques, these experiments provide evidence for such spinally generated units and for the localization of the networks responsible for producing them within different regions of the spinal cord. Such an organization might help to simplify the production of movement, reducing the degrees of freedom that need to be specified by providing a set of units involved in regulating features common to a range of behaviors.

Simplified and effective motor control based on muscle synergies to exploit musculoskeletal dynamics

The basic hypothesis of producing a range of behaviors using a small set of motor commands has been proposed in various forms to explain motor behaviors ranging from basic reflexes to complex voluntary movements. Yet many fundamental questions regarding this long-standing hypothesis remain unanswered. Indeed, given the prominent nonlinearities and high dimensionality inherent in the control of biological limbs, the basic feasibility of a low-dimensional controller and an underlying principle for its creation has remained elusive. We propose a principle for the design of such a controller, that it endeavors to control the natural dynamics of the limb, taking into account the nature of the task being performed. Using this principle, we obtained a low-dimensional model of the hindlimb and a set of muscle synergies to command it. We demonstrate that this set of synergies was capable of producing effective control, establishing the viability of this muscle synergy hypothesis. Finally, by combining the low-dimensional model and the muscle synergies we were able to build a relatively simple controller whose overall performance was close to that of the systems full-dimensional nonlinear controller. Taken together, the results of this study establish that a low-dimensional controller is capable of simplifying control without degrading performance.

Gap junctions and motor behavior

The production of any motor behavior requires coordinated activity in motor neurons and premotor networks. In vertebrates, this coordination is often assumed to take place through chemical synapses. Here we review recent data suggesting that electrical gap-junction coupling plays an important role in coordinating and generating motor outputs in embryonic and early postnatal life. Considering the recent demonstration of a prevalent expression of gap-junction proteins and gap-junction structures in the adult mammalian spinal cord, we suggest that neuronal gap-junction coupling might also contribute to the production of motor behavior in adult mammals.