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.
Brain machine interface (BMI) systems hold the potential to return lost functions to patients with motor disorders. Currently most efforts in BMI have concentrated on decoding neural activity from forearm areas of cortex to operate a robotic arm or perform other manipulation tasks. Efforts have neglected the locomotion functions of hindlimb / trunk cortex. However, the role of cortex in hindlimb locomotion of intact rats, which are often model systems for BMI testing, is usually considered to be small. Thus, the quality of representations of locomotion available in this area was uncertain. We designed a new rodent BMI system, and tested decoding of the kinematics of trunk and hindlimbs during locomotion using linear regression. Recordings were made from the motor cortex of the hindlimb / trunk area in rats using arrays of 6 tetrodes (24 channels total). We found that multiple movement related variables could be decoded simultaneously during locomotion, ranging from the proximal robot / pelvis attachment point, and the distal toe position, through hindlimb joint angles and limb endpoint in a polar coordinate system. Remarkably, the best reconstructed motion parameters were the more proximal kinematics, which might relate to global task variables. The pelvis motion was significantly better reconstructed than any other motion features.
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.
Neonatal spinalized (NST) rats can achieve autonomous weight supported locomotion never seen after adult injury. Mechanisms that support function in NST rats include increased importance of cortical trunk control, and altered biomechanical control strategies for stance and locomotion. Hindlimbs are isolated from perturbations in quiet stance and act in opposition to forelimbs in locomotion in NST rats. Control of roll and yaw of the hindlimbs is crucial in their locomotion. The biomechanics of the hind limbs of NST rats are also likely crucial. We present new data showing the whole leg musculature scales proportional to normal rat musculature in NST rats, regardless of function. This scaling is a prerequisite for the NST rats to most effectively use pattern generation mechanisms and motor patterns that are similar to those present in intact rats. Pattern generation may be built into the lumbar spinal cord by evolution and matched to the limb biomechanics, so preserved muscle scaling may be essential to the NST function observed.
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