Corey B. Hart

Modular Premotor Drives and Unit Bursts as Primitives for Frog Motor Behaviors

Spinal cord modularity impacts on our understanding of reflexes, development, descending systems in normal motor control, and recovery from injury. We used independent component analysis and best-basis or matching pursuit wavepacket analysis to extract the composition and temporal structure of bursts in hindlimb muscles of frogs. These techniques make minimal a priori assumptions about drive and motor pattern structure. We compared premotor drive and burst structures in spinal frogs with less reduced frogs with a fuller repertoire of locomotory, kicking, and scratching behaviors. Six multimuscle drives explain most of the variance of motor patterns (∼80%). Each extracted drive was activated with pulses at a single time scale or common duration (∼275 msec) burst structure. The data show that complex behaviors in brainstem frogs arise as a result of focusing drives to smaller core groups of muscles. Brainstem drives were subsets of the muscle groups from spinal frogs. The 275 msec burst duration was preserved across all behaviors and was most precise in brainstem frogs. These data support a modular decomposition of frog behaviors into a small collection of unit burst generators and associated muscle drives in spinal cord. Our data also show that the modular organization of drives seen in isolated spinal cord is fine-tuned by descending controls to enable a fuller movement repertoire. The unit burst generators and their associated muscle synergies extracted here link the biomechanical “primitives,” described earlier in the frog, rat, and cat, and to the elements of pattern generation examined in fictive preparations.

A Neural Basis for Motor Primitives in the Spinal Cord

Motor primitives and modularity may be important in biological movement control. However, their neural basis is not understood. To investigate this, we recorded 302 neurons, making multielectrode recordings in the spinal cord gray of spinalized frogs, at 400, 800, and 1200 μm depth, at the L2/L3 segment border. Simultaneous muscle activity recordings were used with independent components analysis to infer premotor drive patterns. Neurons were divided into groups based on motor pattern modulation and sensory responses, depth recorded, and behavior. The 187 motor pattern modulated neurons recorded comprised 14 cutaneous neurons and 28 proprioceptive neurons at 400 μm in the dorsal horn, 131 intermediate zone interneurons from ∼800 μm depth without sensory responses, and 14 motoneuron-like neurons at ∼1200 μm. We examined all such neurons during spinal behaviors. Mutual information measures showed that cutaneous neurons and intermediate zone neurons were related better to premotor drives than to individual muscle activity. In contrast, proprioceptive-related neurons and ventral horn neurons divided evenly. For 46 of the intermediate zone interneurons, we found significant postspike facilitation effects on muscle responses using spike-triggered averages representing short-latency postspike facilitations to multiple motor pools. Furthermore, these postspike facilitations matched significantly in both their patterns and strengths with the weighting parameters of individual primitives extracted statistically, although both were initially obtained without reference to one another. Our data show that sets of dedicated interneurons may organize individual spinal primitives. These may be a key to understanding motor development, motor learning, recovery after CNS injury, and evolution of motor behaviors.

Primitives, premotor drives, and pattern generation: a combined computational and neuroethological perspective.

A modular motor organization may be needed to solve the degrees of freedom problem in biological motor control. Reflex elements, kinematic primitives, muscle synergies, force-field primitives and/or pattern generators all have experimental support as modular elements. We discuss the possible relations of force-field primitives, spinal feedback systems, and pattern generation and shaping systems in detail, and review methods for examining underlying motor pattern structure in intact or semi-intact behaving animals. The divisions of systems into primitives, synergies, and rhythmic elements or oscillators suggest specific functions and methods of construction of movement. We briefly discuss the limitations and caveats needed in these interpretations given current knowledge, together with some of the hypotheses arising from these frameworks.

A Simple Experimentally Based Model Using Proprioceptive Regulation of Motor Primitives Captures Adjusted Trajectory Formation in Spinal Frogs

Spinal circuits may organize trajectories using pattern generators and synergies. In frogs, prior work supports fixed-duration pulses of fixed composition synergies, forming primitives. In wiping behaviors, spinal frogs adjust their motor activity according to the starting limb position and generate fairly straight and accurate isochronous trajectories across the workspace. To test whether a compact description using primitives modulated by proprioceptive feedback could reproduce such trajectory formation, we built a biomechanical model based on physiological data. We recorded from hindlimb muscle spindles to evaluate possible proprioceptive input. As movement was initiated, early skeletofusimotor activity enhanced many muscle spindles firing rates. Before movement began, a rapid estimate of the limb position from simple combinations of spindle rates was possible. Three primitives were used in the model with muscle compositions based on those observed in frogs. Our simulations showed that simple gain and phase shifts of primitives based on published feedback mechanisms could generate accurate isochronous trajectories and motor patterns that matched those observed. Although on-line feedback effects were omitted from the model after movement onset, our primitive-based model reproduced the wiping behavior across a range of starting positions. Without modifications from proprioceptive feedback, the model behaviors missed the target in a manner similar to that in deafferented frogs. These data show how early proprioception might be used to make a simple estimate initial limb state and to implicitly plan a movement using observed spinal motor primitives. Simulations showed that choice of synergy composition played a role in this simplicity. To generate froglike trajectories, a hip flexor synergy without sartorius required motor patterns with more proprioceptive knee flexor control than did patterns built with a more natural synergy including sartorius. Such synergy choices and control strategies may simplify the circuitry required for reflex trajectory construction and adaptation.

Motor primitives and synergies in the spinal cord and after injury—the current state of play

Modular pattern generator elements, also known as burst synergies or motor primitives, have become a useful and important way of describing motor behavior, albeit controversial. It is suggested that these synergy elements may constitute part of the pattern‐shaping layers of a McCrea/Rybak two‐layer pattern generator, as well as being used in other ways in the spinal cord. The data supporting modular synergies range across species including humans and encompass motor pattern analyses and neural recordings. Recently, synergy persistence and changes following clinical trauma have been presented. These new data underscore the importance of understanding the modular structure of motor behaviors and the underlying circuitry to best provide principled therapies and to understand phenomena reported in the clinic. We discuss the evidence and different viewpoints on modularity, the neural underpinnings identified thus far, and possible critical issues for the future of this area.

Spinal cord modularity: evolution, development, and optimization and the possible relevance to low back pain in man

The words of Hughlings Jackson in 1884 were inspired by a consideration of what was then the recent work of Darwin on evolution. In the quoted article he applied this perspective to CNS evolution, development and subsequent neurological damage. His overall framework likely remains relevant today. Our paper’s goal is to review current perspectives on motor modularity and its mechanisms, especially at the spinal level (for Jackson ‘well-organized’, ‘simpler’ and ‘more automatic’), but also beyond. Modularity can be defined as the use of designs employing standardized components or units, allowing easy assembly, repair and flexible arrangements of the components. The simplest modules in a system, from which other larger modules might be made, can be termed primitives. This term derives from a combination of the biological definition of primitive as ‘occurring in or characteristic of an early stage of development or evolution’, the definition of primitive as an element assumed as a basis, and the computer science definition of ‘a basic or fundamental unit of machine instruction’. Like Jackson, we will argue that these modules and primitives are in significant part already organized at birth. At the end of this review, we discuss how these issues in spinal modularity and protective reflex structure may relate to trunk control and low back pain mechanisms in humans.

Distinguishing synchronous and time-varying synergies using point process interval statistics: motor primitives in frog and rat

We present and apply a method that uses point process statistics to discriminate the forms of synergies in motor pattern data, prior to explicit synergy extraction. The method uses electromyogram (EMG) pulse peak timing or onset timing. Peak timing is preferable in complex patterns where pulse onsets may be overlapping. An interval statistic derived from the point processes of EMG peak timings distinguishes time-varying synergies from synchronous synergies (SS). Model data shows that the statistic is robust for most conditions. Its application to both frog hindlimb EMG and rat locomotion hindlimb EMG show data from these preparations is clearly most consistent with synchronous synergy models (p < 0.001). Additional direct tests of pulse and interval relations in frog data further bolster the support for synchronous synergy mechanisms in these data. Our method and analyses support separated control of rhythm and pattern of motor primitives, with the low level execution primitives comprising pulsed SS in both frog and rat, and both episodic and rhythmic behaviors.