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Limb position sense: Role of limb posture, visual experience, and input from muscle spindle Ia afferents

2019-04-02 , Oh, Kyunggeune

Limb position sense is the ability to determine location and orientation of limb segments with respect to each other and with respect to the external environment without vision. Limb position sense is critical for accurate control of posture and movement. The lack of position sense due to illness has devastating consequences for the performance of even simplest motor tasks performed under visual control. Position sense of limb segments with respect to each other originates from joint angle-related sensory information provided by the muscle spindles, Golgi tendon organs and cutaneous afferents in skin overlying joints. Limb endpoint position sense with respect to external space can be derived by the nervous system through a transformation of joint-related coordinates to endpoint external coordinates using estimated dimensions of limb segments. This coordinate transformation and factors that can potentially affect accuracy and precision of endpoint position sense in external space are not fully understood, and many important questions remain unanswered. For example, it is not clear why people perceive hand position more precisely in the radial than in azimuth direction and closer to the body than farther away. Moreover, since vision contributes to forming somatosensory representations of body segment dimensions and to integration of somatosensory information encoded in joint-based and external coordinates, would long-term blindness differentially affect the limb position sense in joint and external space coordinates? Furthermore, what does happen to precision of limb endpoint positioning in external space if input from muscle spindle Ia afferents from a major limb joint is compromised? My work addressed all these questions. Using a theoretical analysis of the transformation of random joint angle errors to random hand position errors for a two-joint kinematic arm model, I demonstrated that arm posture alone can explain the better precision of hand position sense in the radial than in azimuth direction and closer to the body than farther away. I confirmed the model predictions in experiments with healthy sighted individuals (n=11) who performed a hand position matching task. The fact that the predicted distributions of random hand position errors (precision ellipses) in the horizontal workspace were nearly orthogonal to the experimentally obtained arm stiffness ellipses reported in the literature, provides a mechanistic explanation for how the distribution of random hand position errors is shaped for any arm posture. To investigate the role of visual experience in arm position sense in joint and external space coordinates, I investigated long-term blind (n=7) and age-matched sighted individuals (n=7) who performed three arm position matching tasks: joint angle matching (JAM), hand distance and direction matching (DDM), and hand distance and mirror direction matching (MDDM). The latter hand position matching task was kinematically identical to the joint angle matching task JAM. The blind participants generally had lower accuracy and precision of arm position sense in joint angle and hand position matching than the sighted. In addition, the blind had the same precision of arm position sense in the joint angle matching and hand position matching tasks. Measuring the Contingent Negative Variation-inspired EEG potential (CNV), an indicator of neurophysiological functions related to task complexity during the performance of arm matching tasks, revealed that the blind group had a higher EEG negative potential than the sighted group. Both subject groups demonstrated a higher EEG negative potential in the hand position matching DDM task than in the joint angle JAM task or in another hand position matching MDDM. These results suggest that visual experience positively affects arm position sense possibly due to integration of visual and proprioceptive sensory information and the development of more accurate body schema. I suggest that similar precision of arm position sense in joint and external coordinates in the blind participants may result from a possible increase in perceptual acuity of other exteroceptors that could provide information about limb position in the peripersonal space. The lower accuracy and higher perceived task complexity in the DDM task, as judged from the EEG negative potential, may indicate more complex transformations from the joint coordinates to hand position coordinates required for this task. In the last series of experiments, I investigated precision of hindpaw position control just before and right after the stance phase during walking in 4 cats after their major knee muscles were self-reinnervated unilaterally. This procedure compromises sensory input from Ia afferents (Cope at al. 1994), the main source of joint-related position information. Contrary to my expectations, the precision of paw position control at the late and mid-swing phase during walking significantly increased bilaterally. The animals achieved this by adopting a more extended hindlimb posture bilaterally during mid-swing and prior to stance onset. This extended limb posture reduces the radial random error, as follows from my theoretical analysis of precision of limb position sense. These studies determined for the first time the contribution of limb posture, visual experience and proprioceptive input to accuracy and precision of limb position sense. This information will help design new diagnostic and therapeutic tools for people with visual and proprioceptive deficits. The gained understanding of random error distributions of hand position sense can be used to design control panels for blind and sighted operators that increase precision and accuracy of control.

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Dynamic stability of quadrupedal locomotion: animal model, cortical control and prosthetic gait

2012-11-13 , Farrell, Bradley J.

The ability to control balance and stability are essential to prevent falls during locomotion. Maintenance of stable locomotion is challenging especially when complicated by amputation and prosthesis use. Humans employ several motor strategies to maintain stability during walking on complex terrain: decreasing walking speed, adjusting stride length and stance width, lowering the center of mass, and prolonging the double support time. The mechanisms of selecting these motor strategies by the primary motor cortex are unknown and cannot be studied directly in humans. There is also little information about dynamic stability of prosthetic gait with bone-anchored prostheses, which are thought to provide sensory feedback to the amputee through osseoperception. Therefore, the Specific Aims of my research were to (1) evaluate dynamic stability and the activity of the primary motor cortex during walking with different constraints on the base of support and (2) develop an animal model to evaluate mechanics and stability of prosthetic gait with a bone-anchored prosthesis. To address these aims, I developed a feline model that allows for investigating (1) the role of the primary motor cortex in regulation of dynamic stability of intact locomotion, (2) skin and bone integration with a percutaneous porous titanium implant facilitating prosthetic attachment, and (3) dynamic stability of walking on a bone-anchored prosthesis. The results of Specific Aim 1 demonstrated that the area and shape of the base of support influence the margins of dynamic stability during quadrupedal walking. For example, I found that the animal is dynamically unstable in the sagittal plane and frontal plane (although to a lesser degree) during a double-support by a forelimb and the contralateral hindlimb. Elevated neuronal activity from the right forelimb representation in the primary motor cortex during these phases suggests that the motor cortex may contribute to selection of paw placement location and thus to regulation of stability. The results of Specific Aim 2 on the development of skin-integrated bone-anchored prostheses demonstrated the following. Skin ingrowth into 3 types of porous titanium pylons (pore sizes 40-100 μm and 100-160 μm and nano-tubular surface treatment) implanted under skin of rats was seen 3 and 6 weeks after implantation, and skin filled at least 30% of available implant space. The duration of implantation, but not implant pore size (in the studied range) or surface treatment statistically influenced skin ingrowth; pore size and time of implantation affected the implant extrusion length (p<0.05). The implant type with the slowest extrusion rate (pore size 40-100 μm) was used in a feline model of prosthetic gait with skin-integrated bone-anchored prosthesis. The developed implantation methods, rehabilitation procedures and feline prostheses allowed 2 animals to utilize skin- and bone-integrated prostheses for dynamically stable locomotion. Prosthetic gait analysis demonstrated that the animals loaded the prosthetic limb, but increased reliance on intact limbs for weight support and propulsion. The obtained results and developed animal model improve the understanding of locomotor stability control and integration of skin with percutaneous implants.

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Quadrupedal locomotion with a unilateral bone-anchored transtibial prosthesis in the cat

2017-11-10 , Jarrell, Joshua Ryan

Bone-anchored limb prostheses offer numerous advantages over conventional socket-supported prostheses. As opposed to socket prostheses, loads on a bone-anchored prosthetic limb during natural activities are directly transmitted to the residual bone, which prevents damage of skin and other soft tissues. Despite this and other documented advantages, however, bone-anchored prostheses have been limited in their availability in the United States due to an increased risk of skin and deep tissue infection through the skin-implant interface. A novel porous titanium pylon, the skin- and bone-integrating pylon (SBIP), has been developed to promote deeper tissue integration with the percutaneous implant and thereby reduce the risk of infection (Farrell et al., 2014c; Pitkin et al., 2009; Pitkin, 2012). Further research is needed to examine if the SBIP can be utilized for anchoring a limb prosthesis in natural load bearing applications. In veterinary medicine, gait changes in animals after limb loss and subsequent prosthesis intervention have not been extensively investigated. In addition, it is not completely understood how the motor system adapts to a loss of sensory feedback from the distal leg and to a reduced ability to absorb and generate mechanical energy for locomotion. Currently, detailed biomechanical analyses of such adaptations are missing. Therefore, the overall goal of my research was to investigate the effects of walking with a unilateral, transtibial, bone-anchored via SBIP prosthesis on mechanics and stability of quadrupedal locomotion and on tissue integration with the SBIP implant. The general hypothesis tested was that the SBIP would provide secure, infection free anchoring of a transtibial prosthesis and that would permit the cats to adopt the prosthesis for stable quadrupedal locomotion. In Specific Aim 1, I examined the ability of the SBIP to serve as attachment for a unilateral, transtibial bone-anchored prosthesis during walking in the cat. In Specific Aim 2, I investigated dynamic stability by analyzing margins of dynamic stability and changes in angular impulse during quadrupedal walking with a unilateral bone-anchored passive transtibial prosthesis. In Specific Aim 3, I determined the amount of skin and bone ingrowth into the SBIP after the residual tibia had been loaded during natural motor activities including level and slope walking. The results of these investigations showed purposeful adoption of the bone-anchored prosthesis into the animals’ chosen gait strategies. More specifically, normal ground reaction forces produced by the prosthetic limb were of substantial magnitudes (at least 50% of the pre implantation level), and tangential ground reaction forces, while significantly reduced, were statistically greater than zero and in the appropriate direction and timing across the gait cycle. Frontal-plane stability metrics deviated from the intact values to a lesser extent than in similar studies in human prosthetic gait. The histological results revealed deep bone and skin integration highly correlated with the duration of implantation and exceeded ingrowth of in a non-locomotive subject of similar implantation times. This study has provided important new information about the ability of the novel SBIP implants to be utilized for anchoring limb prostheses and about how the motor system of a quadrupedal animal adapts to a partial loss of the limb’s ability to absorb and generate mechanical energy for locomotion.

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Motor control in persons with a trans-tibial amputation during cycling

2011-07-06 , Childers, Walter Lee

Motor control of any movement task involves the integration of neural, muscular and skeletal systems. This integration must occur throughout the sensorimotor system and focus its efforts on controlling the system endpoint, e.g. the foot during locomotion. A person with a uni-lateral trans-tibial amputation has lost the foot, ankle joint, and muscles crossing those joints, hence the residuum becomes the new terminus of the motor system. The amputee must now adjust to the additional challenges of utilizing a compromised motor system as well as the challenges of controlling an external device, i.e. prosthesis, through the mechanical interface between the residuum and prosthetic socket. The obvious physical and physiologic asymmetries between the sound and amputated limbs are also involved in strategies for locomotion involving kinematic and kinetic asymmetries (Winter&Sienko, 1988). There are many questions as to why these asymmetric locomotor strategies are selected and what factors may be influencing that strategy. Factors influencing a change in locomotor strategy could be related to 1) the central nervous system accounting for the loss of sensorimotor feedback, 2) the altered mechanics of this new human/prosthetic system, or some combination of these factors. Understanding how the human motor system adjusts to the amputation and to the addition of an external mechanical device can provide useful insight into how robust the human control system may be and to adaptations in human motor control. This research uses a group of individuals with a uni-lateral trans-tibial amputation and a group of intact individuals using an Ankle Foot Orthosis (AFO) performing a cycling task to understand the "motor adjustments" necessary to utilize an external device for locomotion. Results of these experiments suggest 1) the motor system does account for the activation-contraction dynamics when coordinating muscle activity post amputation, 2) the motor system also changes joint kinetics and muscle activity, 3) these changes are related to control of the interface between the limb and the external device, and 4) the motor system does not alter kinetic asymmetries when kinematic asymmetries are minimized, contrary to a common practice in rehabilitation (Kapp, 2004). Results suggest that control of the external device, i.e. prosthesis or AFO, via the interface between the limb and the device reflect "motor adjustments" made by the nervous system and may be viewed in the context of tool use. Clinical goals in rehabilitation currently focus on minimizing gait deviations whereas the clinical application of these results suggest these deviations from normal locomotion are motor adjustments necessary to control a tool, i.e. prosthesis, by the motor system. Examining amputee locomotion in the context of tool use changes the clinical paradigm from one designed to minimize deviations to one intended to understand this behavior as related to interface control of the device thereby shifting the focus to improving function of the limb/prosthesis system. Kapp SL. (2004) Atlas amp limb def: surg pros rehab princ. 3rd ed: 385 - 394. Winter&Sienko. (1988) J Biomech, 21: 361 - 367.

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Mechanisms of coordination between one- and two-joint synergist muscles

2016-04-15 , Mehta, Ricky

Major muscle groups (e.g. triceps surae, quadriceps, hamstrings, triceps brachii) contain synergist muscles that cross either one or two joints; they are called one- and two-joint muscles. The functional significance of this musculoskeletal design, extensively studied in the past, has been suggested to increase the economy and efficiency of movement. Much less attention has been paid to the mechanisms responsible for the differential activation, or coordination, between one- and two-joint synergists. The understanding of these mechanisms will not only add to the basic knowledge of neural control of movement but also contribute to prevention and therapeutic interventions of muscle injuries that often occur in two-joint muscles. Previous work has suggested that mechanical intermuscular interactions, resultant muscle moment requirements at the adjacent joints, movement speed, and muscle length-velocity related sensory feedback can affect this coordination. Additionally, the comparison of motoneuronal and muscle activity patterns between fictive and real locomotion in cats suggests a greater influence of motion related sensory feedback on activity of proximal two-joint muscles (i.e., rectus femoris and hamstrings) compared to one-joint muscles and distal two-joint muscles (medial and lateral gastrocnemius). Therefore, the first goal of this work was to test the possible contribution of mechanical intermuscular interactions between one- and two-joint ankle extensors in the cat. The second goal was to examine the role of joint moment requirements, movement speed and length-velocity related feedback in distinct activation of distal one- and two-joint muscles (soleus and gastrocnemius). The third goal was to investigate the effect of removal of length-velocity sensory feedback from proximal one- and two-joint muscles (vastii and rectus femoris) on coordination of these muscles. To address the above goals, an array of motor tasks with different speeds and combinations of joint moments were studied in cats and humans. The tasks included level, downslope and upslope walking and paw shake response in cats, as well as back and leg load lifting and jumping in humans. Motion capture and force plate data were recorded to analyze kinematics and joint moments, sonomicrometry was used to measure muscle fascicle length in cats, and electromyography (EMG) was used to quantify muscle activity. Length-velocity related sensory feedback was removed in cats by muscle self-reinnervation. Results show that mechanical intermuscular interactions via myofascial force transmission should be considered in the coordination between adjacent one- and two-joint synergist muscles in certain pathological conditions leading to increased muscle lengths. Coordination between distal and proximal one- and two-joint synergists depends on joint moment requirements, and the differential inhibition of soleus and excitation of gastrocnemius does not depend on movement speed or length-velocity related sensory feedback. Removal of length-velocity related sensory feedback has a strong effect on coordination between the studied proximal synergist pair (vastii and rectus femoris) but not on coordination of the distal synergist pair (soleus and gastrocnemius). Findings presented here expand on understanding the role of mechanical interactions, sensory feedback and feedforward control in the coordination between one- and two-joint muscles. These findings have potential implications for developing targeted rehabilitation strategies/treatment and implementation of new control strategies for robotics and prosthetics to improve movement efficiency.

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Motor learning and its transfer during bilateral arm reaching.

2011-06-09 , Harley, Linda Rosemary

Have you ever attempted to rub your abdomen with one hand while tapping your head with the other? Separately these movements are easy to perform but doing them together (bilateral task) requires motor adaptation. Motor adaptation is the process through which the Central Nervous System improves upon performance. Transfer of learning is the process through which learning a motor task in one condition improves performance in another condition. The purpose of this study was to determine whether transfer of learning occurs during bilateral goal-directed reaching tasks. It was hypothesized that transfer of learning would occur from the non-dominant to the dominant arm during bilateral tasks and that position and load feedback from the arms would affect the rate of adaptation and transfer of learning. During the experiments, subjects reached with one or both their index finger(s) to eight targets while a velocity dependent force perturbation (force environment) was applied to the arm(s). Three groups of bilateral tasks were examined: (1) unilateral reaching, where one arm learned to reach in a force environment, while the other arm remained stationary and therefore did not provide movement related position or load feedback; (2) bilateral reaching single load, where both arms performed reaching movements but only one arm learned a force environment and therefore the other arm provided movement related position feedback but not load feedback; (3) bilateral reaching two loads, where both arms performed reaching movements and both learned a force environment, while providing movement related position and load feedback. The rate of adaptation of the force environment was quantified as the speed at which the perturbed index finger trajectory became straight over the course of repeated task performance. The rate of adaptation was significantly slower for the dominant arm during the unilateral reaching tasks than during the bilateral reaching single load tasks (p<0.05). This indicates that the movement related position feedback from the non-dominant arm improved significantly the motor adaptation of the dominant arm; therefore transfer of learning occurred from the non-dominant to the dominant arm. The rate of adaptation for the non-dominant arm did not differ significantly (p>0.05) between the unilateral reaching and bilateral reaching single load tasks. Results also indicated that the rate of adaptation was significantly (p<0.05) faster for both the non-dominant and the dominant arms during the bilateral reaching two loads tasks than during the bilateral reaching single load tasks. The latter results indicate that transfer of learning occurred in both directions - from the dominant to the non-dominant arm and from the non-dominant to the dominant arm - when position and load feedback was available from both arms, but only when the force environment acted in the same joint direction. This study demonstrated that transfer of learning does occur during bilateral reaching tasks and that the direction and degree of transfer of learning may be modulated by the position and load feedback that is available to the central nervous system. This information may be used by physical therapists in order to improve rehabilitation strategies for the upper extremity.