William J. Kargo

Individual Premotor Drive Pulses, Not Time-Varying Synergies, Are the Units of Adjustment for Limb Trajectories Constructed in Spinal Cord

Complex actions may arise by combining simple motor primitives. Our studies support individual premotor drive pulses or bursts as execution primitives in spinal cord. Alternatively, the fundamental execution primitives at the segmental level could be time-varying synergies. To distinguish these hypotheses, we examined sensory feedback effects during targeted wiping organized in spinal cord. This behavior comprises three bursts. We tested (1) whether feedback altered the structure of individual premotor drive bursts or primitives, and (2) whether feedback differentially modulated different drive bursts or pulses in the three burst sequence. At least two of the three bursts would need to always be comodulated to support a time-varying synergy. We used selective muscle vibration to control spindle feedback from a single muscle (biceps/iliofibularis). The structures of premotor drive bursts were conserved. However, biceps vibration (1) scaled the amplitudes of two bursts coactivated during the initial phase of wiping independently of one another without altering their phase, and (2) independently phase regulated the third burst but preserved its amplitude. Thus, all three bursts were regulated separately. Durations were unaffected. The independent effects depended on (1) time of vibration during wiping, (2) frequency of vibration, and (3) limb configuration. Because each of the three bursts was independently modulated, these data strongly support execution using individual premotor bursts rather than time-varying synergies at the spinal level of motor organization. Our data show that both sensory feedback and central systems of the spinal cord act in concert to adjust the individual premotor bursts in support of the straight and unimodal wiping trajectory.

Improvements in the Signal-to-Noise Ratio of Motor Cortex Cells Distinguish Early versus Late Phases of Motor Skill Learning

There are numerous experience-driven changes in cortical circuitry that correlate with improved performance. Improved motor performance on a reach-to-grasp task in rodents is associated with changes in long-term potentiation (LTP), synaptogenesis, and movement representations in primary motor cortex (M1) by training days 3, 7, and 10, respectively. We recorded single-cell activity patterns in M1 during reach-to-grasp training to test how neural-spiking properties change with respect to LTP, synaptogenesis, and motor map changes. We also tested how neural-spiking changes relate directly to improved performance by monitoring muscle activity patterns. We found that signal-to-noise ratios (SNRs) of M1 spiking were significantly improved with practice but only after 7-12 d. Three sources of noise were assessed: signal-dependent noise exemplified by the slope of the relationship between mean spike count and count variance per burst, signal-independent noise exemplified by the offset of this relationship, and background firing rates before and after bursts. Signal-independent noise and pre-burst firing rates were reduced with practice. Early performance gains (days 1-6) were dissociated from SNR improvements, whereas later performance gains (day 7-12) were related directly to the magnitude of improvement in both muscle recruitment reliability and success rates. With training, an increased number of cells exhibited firing rates that were correlated with muscle recruitment patterns, with lags suggesting a primary direction of influence from M1 to muscles. These results suggest a functional linkage from local synaptogenesis in M1 to improved spiking reliability of M1 cells to more reliable recruitment of muscles and finally to improved behavioral performance.

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.

Conserved temporal dynamics and vector superposition of primitives in frog wiping reflexes during spontaneous extensor deletions

Abstract We use spontaneous motor pattern deletions in spinal frogs to test a computational theory of movement construction. We hypothesize that at the spinal level, operating in isolation from the brain, the forces driving movements are constructed from summation of force-field primitives of fixed temporal dynamics, which can be expressed in the form F(r, r ,t)= ∑ i A i a(t+τ i )φ i (r, r ) where Ai is a scaling parameter, a(t) is a common timing dynamics for each primitive, time shifted for each by ti and φ(r, r ) are functions of limb state. In deletions, the force amplitudes, force directions and patterns behave as predicted by this model of movement construction based on summation of force-field primitives.

Adaptation of Prefrontal Cortical Firing Patterns and Their Fidelity to Changes in Action–Reward Contingencies

Animals adapt action-selection policies when the relationship between possible actions and associated outcomes changes. Prefrontal cortical neurons vary their discharge patterns depending on action choice and rewards received and undoubtedly play a pivotal role in maintaining and adapting action policies. Here, we recorded neurons from the medial precentral subregion of mouse prefrontal cortex to examine neural substrates of goal-directed behavior. Discharge patterns were recorded after animals developed stable action-selection policies, wherein four possible action sequences were invariably related to different reward magnitudes and during adaptation to changes in the action–reward contingencies. During the adaptation period, when the same action sequence resulted in different reward magnitudes, many neurons (38%) exhibited significantly different discharge patterns for identical action sequences, well before reaching the reward site. In addition, trial-to-trial reliability of ensemble pattern production leading up to reward was found to vary both positively and negatively with increases and decreases in reward magnitude, respectively. Pairwise analyses of simultaneously recorded neurons revealed that decreased reliability in part reflected fluctuations between different ensemble activity patterns as opposed to within-pattern variability. Increases in reliability were related to an increased probability of both selecting highly rewarding actions and completing such actions without pause or reversal, whereas decreases in reliability were associated with the opposite pattern. Thus, we suggest that both the spatiotemporal pattern and fidelity of prefrontal cortical discharge are impacted by action–outcome relationships and that each of these features serve to adapt action choices and maintain behaviors leading to reward.

Trunk Sensorimotor Cortex Is Essential for Autonomous Weight-Supported Locomotion in Adult Rats Spinalized as P1/P2 Neonates

Unlike adult spinalized rats, approximately 20% of rats spinalized as postnatal day 1 or 2 (P1/P2) neonates achieve autonomous hindlimb weight support. Cortical representations of mid/low trunk occur only in such rats with high weight support. However, the importance of hindlimb/trunk motor cortex in function of spinalized rats remains unclear. We tested the importance of trunk sensorimotor cortex in their locomotion using lesions guided by cortical microstimulation in P1/P2 weight-supporting neonatal spinalized rats and controls. In four intact control rats, lesions of hindlimb/trunk cortex caused no treadmill deficits. All spinalized rats lesioned in trunk cortex (n = 16: 4 transplant, 6 transect, 6 transect + fibrin glue) lost an average of about 40% of their weight support. Intact trunk cortex was essential to their level of function. Lesion of trunk cortex substantially increased roll of the hindquarters, which correlated to diminished weight support, but other kinematic stepping parameters showed little change. Embryonic day 14 (E14) transplants support development of the trunk motor representations in their normal location. We tested the role of novel relay circuits arising from the grafts in such cortical representations in E14 transplants using the rats that received (noncellular) fibrin glue grafting at P1/P2 (8 allografts and 32 xenografts). Fibrin-repaired rats with autonomous weight support also had trunk cortical representations similar to those of E14 transplant rats. Thus acellular repair and intrinsic plasticity were sufficient to support the observed features. Our data show that effective cortical mechanisms for trunk control are essential for autonomous weight support in P1/P2 spinalized rats and these can be achieved by intrinsic plasticity.

Modeling of dynamic controls in the frog wiping reflex: Force-field level controls

Abstract We compare free-limb kinematics in deafferented and afferented spinal frogs and use a dynamic model to generate model kinematics driven by isometric force-field patterns from the same animals for comparison. Afferented paths in simulation and experiment agree over 50% of their extent. Results suggest that frogs use sensory information to construct force-fields that minimize the need for eccentric muscle contractions during movement, but such eccentric contractions in deafferented frogs compensate interaction torques. The simulation data support movement construction as an adjusted combination of force-field primitives and demonstrate the importance of non-isometric properties of the force-field primitive.

Dopamine signaling and the distal reward problem

Actions and their associated consequences, such as reward attainment, are often temporally distant. Animals nevertheless learn such associations thereby solving the ‘distal reward’ problem. We sought to determine whether dopamine signaling plays a role in such learning. Wild-type and dopamine type I receptor knockout mice executed three left/right choices leading to one of eight differentially rewarded goal sites. Compared with wild-type mice, knockouts exhibited selective impairments in decision making at choice points distal, but not proximal, to goal sites. We conclude that dopamines role in reinforcement learning depends on the temporal relationship of actions to reward and that dopamine signaling through D1 receptors constitutes a component of those brain mechanisms responsible for solving the distal reward problem.

Movement Organization in the Frog Spinal Cord: Prerational Intelligence?

This article will present a particular view of pre-rational intelligence as it pertains to pieces of neural circuitry. The subject of this article is the spinal cord. This is only a subsystem within the nervous system, albeit a critical one. Clearly, adaptive and fully intelligent behavior is only the domain of the full organism (see McFarland & Houston 1981; McFarland & Bosser 1994). However, it seems that some measure of ‘intelligent’ function can be ascribed to a neural subsystem. For the purpose of this discussion we will define an intelligent design and intelligent function of neural subsystems as those that minimize the whole organism’s computational load while maximizing the breadth of the system’s output possibilities. The outputs should clearly be of utility to the organism in the context of other neural systems. There is a trade-off between the two competing goals of flexibility and simplicity. We would suggest that optimizing this trade-off in an organism’s various neural subsystems must frequently involve modularity, encapsulation of function and restriction of system structures to designs that support extensibility. Dimensionality reduction at the interface of the subsystem with others is desirable since this reduces computation in other parts of the nervous system. Autonomous computation within neural modules is desirable to support asynchronous activation, concurrence, and extensibility and flexibility of the system.