Neuromechanical Tuning for Arm Motor Control

Movement is a fundamental behavior that allows us to interact with the external world. Its importance to human health is most evident when it becomes impaired due to disease or injury. Physical and occupational rehabilitation remains the most common treatment for these types of disorders. Although therapeutic interventions may improve motor function, residual deficits are common for many pathologies, such as stroke. The development of novel therapeutics is dependent upon a better understanding of the underlying mechanisms that govern movement. Movement of the human body adheres to the principles of classic Newtonian mechanics. However, due to the inherent complexity of the body and the highly variable repertoire of environmental contexts in which it operates, the musculoskeletal system presents a challenging control problem and the onus is on the central nervous system to reliably solve this problem. The neural motor system is comprised of numerous efferent and afferent pathways with a hierarchical organization which create a complex arrangement of feedforward and feedback circuits. However, the strategy that the neural motor system employs to reliably control these complex mechanics is still unknown. This dissertation will investigate the neural control of mechanics employing a “bottom-up” approach. It is organized into three research chapters with an additional introductory chapter and a chapter addressing final conclusions. Chapter 1 provides a brief description of the anatomical and physiological principles of the human motor system and the challenges and strategies that may be employed to control it. Chapter 2 describes a computational study where we developed a musculoskeletal model of the upper limb to investigate the complex mechanical interactions due to muscle geometry. Muscle lengths and moment arms contribute to force and torque generation, but the inherent redundancy of these actuators create a high-dimensional control problem. By characterizing these relationships, we found mechanical coupling of muscle lengths which the nervous system could exploit. Chapter 3 describes a study of muscle spindle contribution to muscle coactivation using a computational model of primary afferent activity. We investigated whether these afferents could contribute to motoneuron recruitment during voluntary reaching tasks in humans and found that afferent activity was orthogonal to that of muscle activity. Chapter 4 describes a study of the role of the descending corticospinal tract in the compensation of limb dynamics during arm reaching movements. We found evidence that corticospinal excitability is modulated in proportion to muscle activity and that the coefficients of proportionality vary in the course of these movements. Finally, further questions and future directions for this work are discussed in the Chapter 5

Firing properties of muscle spindles supplying the intrinsic muscles of the foot in unloaded and free-standing humans

Human posture and locomotion are dependent on the sensory apparatus – involving muscle spindles, cutaneous afferents and the vestibular system – that provides proprioception. In my previous work with my Bachelor of Medical Research, I investigated the relationship between galvanic vestibular stimulation and the sensitivity of muscle spindles of the long muscles of the leg. While that study showed no correlation between these systems it was limited by the lack of subject postural threat. In order to record from muscle spindles directly during unsupported free-standing, a new methodology for microneurographic recording from the posterior tibial nerve at the ankle was developed. For the first time, we have been able to identify the firing properties of muscle spindle endings in the small (intrinsic) muscles of the foot, as well as mechanoreceptors in the skin of the sole, while the participant is standing unsupported. This thesis presents this methodology along with the recordings made. In Study 1, the firing properties of 26 muscle spindles supplying the intrinsic muscles of the foot are described in unloaded conditions. Their responsiveness to stretch and related joint movements is shown to be similar to those in the short muscles in the hand and the long leg muscles. Only 27% were spontaneously active, of which there was no consistent resting firing rate or discharge variability. In Study 2, activity from 12 muscle spindles supplying the intrinsic foot muscles in unsupported free-standing conditions is described. In this group 50% were spontaneously firing and 67% had activity correlated with changes of centre of pressure recorded by a force plate, primarily (88%) along the anteroposterior axis. In Study 3, the activity of 28 multiunit cutaneous afferent recordings, as well as of 15 single-unit cutaneous afferents, supplying the sole of the foot in unsupported free standing is described. Activity of cutaneous afferents was found to be dependent on receptor type and location of receptive field. The data presented in this report is proof of this novel methodology’s suitability for detailed study into the sensory sources in the foot contributing to maintaining the upright posture

Proprioceptive disturbances in weightlessness revisited

The senses of limb position and movement become degraded in low gravity. One explanation is a gravity-dependent loss of fusimotor activity. In low gravity, position and movement sense accuracy can be recovered if elastic bands are stretched across the joint. Recent studies using instrumented joysticks have confirmed that aiming and tracking accuracy can be recovered in weightlessness by changing viscous and elastic characteristics of the joystick. It has been proposed that the muscle spindle signal, responsible for generating position sense in the mid-range of joint movement, is combined with input from joint receptors near the limits of joint movement to generate a position signal that covers the full working range of the joint. Here it is hypothesised that in low gravity joint receptors become unresponsive because of the loss of forces acting on the joint capsule. This leads to a loss of position and movement sense which can be recovered by imposing elastic forces across the joint

Remembering Forward: Neural Correlates of Memory and Prediction in Human Motor Adaptation

We used functional MR imaging (FMRI), a robotic manipulandum and systems identification techniques to examine neural correlates of predictive compensation for spring-like loads during goal-directed wrist movements in neurologically-intact humans. Although load changed unpredictably from one trial to the next, subjects nevertheless used sensorimotor memories from recent movements to predict and compensate upcoming loads. Prediction enabled subjects to adapt performance so that the task was accomplished with minimum effort. Population analyses of functional images revealed a distributed, bilateral network of cortical and subcortical activity supporting predictive load compensation during visual target capture. Cortical regions – including prefrontal, parietal and hippocampal cortices – exhibited trial-by-trial fluctuations in BOLD signal consistent with the storage and recall of sensorimotor memories or “states” important for spatial working memory. Bilateral activations in associative regions of the striatum demonstrated temporal correlation with the magnitude of kinematic performance error (a signal that could drive reward-optimizing reinforcement learning and the prospective scaling of previously learned motor programs). BOLD signal correlations with load prediction were observed in the cerebellar cortex and red nuclei (consistent with the idea that these structures generate adaptive fusimotor signals facilitating cancelation of expected proprioceptive feedback, as required for conditional feedback adjustments to ongoing motor commands and feedback error learning). Analysis of single subject images revealed that predictive activity was at least as likely to be observed in more than one of these neural systems as in just one. We conclude therefore that motor adaptation is mediated by predictive compensations supported by multiple, distributed, cortical and subcortical structures

The effects of body orientation and humeral elevation angle on shoulder muscle activity and shoulder joint position sense

The purpose of this study was to determine the effects of body tilt on shoulder muscle activity and repositioning accuracy during humeral elevation to three positions in the sagittal plane (70, 90 and 110 degrees). Thirty eight subjects underwent testing in an unconstrained joint position sense task. Kinematics were measured with a magnetic tracking device while muscle activation was measured with surface electromyography. The joint position sense task consisted of subjects moving their arms to a predetermined positing in space with the help of visual feedback from a head mounted display interfaced with the magnetic tracking device. Subjects were then asked to reproduce the presented shoulder position in the absence of visual feedback. The protocol was performed under two tilts: upright and back 90 degrees from vertical. This allowed for the comparison of joint position sense at the same elevation angles but different levels of shoulder muscle activation by altering the orientation of the subjects in the gravitational field. When comparing these two tilts we found that subjects matched with greater accuracy and precision at 90 and 110 degrees of elevation when they were upright (p \u3c 0.05). We also found that anterior deltoid muscle activity was significantly greater at all three elevation angles in the upright condition. This data, when taken together support the hypothesis that unconstrained shoulder joint position sense is enhanced with increased muscular activation levels

Coding of position by simultaneously recorded sensory neurones in the cat dorsal root ganglion

Journal ArticleMuscle, cutaneous and joint afferents continuously signal information about the position and movement of individual joints. How does the nervous system extract more global information, for example about the position of the foot in space? To study this question we used microelectrode arrays to record impulses simultaneously from up to 100 discriminable nerve cells in the L6 and L7 dorsal root ganglia (DRG) of the anaesthetized cat. When the hindlimb was displaced passively with a random trajectory, the firing rate of the neurones could be predicted from a linear sum of positions and velocities in Cartesian (x, y), polar or joint angular coordinates. The process could also be reversed to predict the kinematics of the limb from the firing rates of the neurones with an accuracy of 1-2 cm. Predictions of position and velocity could be combined to give an improved fit to limb position. Decoders trained using random movements successfully predicted cyclic movements and movements in which the limb was displaced from a central point to various positions in the periphery. A small number of highly informative neurones (6-8) could account for over 80% of the variance in position and a similar result was obtained in a realistic limb model. In conclusion, this work illustrates how populations of sensory receptors may encode a sense of limb position and how the firing of even a small number of neurones can be used to decode the position of the limb in space