T. Richard Nichols

Electromyographic Responses From the Hindlimb Muscles of the Decerebrate Cat to Horizontal Support Surface Perturbations

The sensory and neural mechanisms underlying postural control have received much attention in recent decades but remain poorly understood. Our objectives were 1) to establish the decerebrate cat as an appropriate model for further research into the sensory mechanisms of postural control and 2) to observe what elements of the postural response can be generated by the brain stem and spinal cord. Ten animals were decerebrated using a modified premammillary technique, which consists of a premammillary decerebration that is modified with a vertical transection near the subthalamic nucleus to eliminate spontaneous locomotion. Horizontal support surface perturbations were applied to all four limbs and electromyographic recordings were collected from 14 muscles of the right hindlimb. Muscle activation was quantified with tuning curves, which compared increases and decreases in muscle activity to background and graphed the difference against perturbation direction. Parallels were drawn between these tuning curves, which were further quantified with a principal direction and breadth (range of directions of muscle activation), and data collected by other researchers from the intact animal. We found a strong similarity in the direction and breadth of the tuning curves generated in the decerebrate and intact cat. These results support our hypothesis that directionally specific tuning of muscles in response to support surface perturbations does not require the cortex, further indicating a strong role for the brain stem and spinal cord circuits in mediating directionally appropriate muscle activation patterns.

The decerebrate cat generates the essential features of the force constraint strategy.

Cats actively respond to horizontal perturbations of the supporting surface according to the force constraint strategy. In this strategy, the force responses fall into two groups oriented in either rostral and medial directions or caudal and lateral directions, rather than in strict opposition to the direction of perturbation. When the distance between forelimbs and hindlimbs is decreased, the responses are less constrained and directed more in line with the perturbation. We have recently shown that electromyographic responses from limb muscles of the decerebrate cat resemble those obtained in the intact animal. Our objectives here were to determine whether the decerebrate cat preparation would also exhibit the force constraint strategy and whether that strategy would exhibit the characteristic dependence on limb position on the strategy. Horizontal support surface perturbations were delivered and three-dimensional exerted forces were recorded from all four limbs. Clustered force responses were generated by all four limbs and were found to be statistically indistinguishable between animals decerebrated using two different levels of transection. The directionality of the force responses was preserved throughout successive time epochs during the perturbations. In addition, the clustering of force responses increased with distance between forelimbs and hindlimbs. These results indicate that the force constraint strategy used by terrestrial animals to maintain stability can be generated without the assistance of the cerebral cortices and without prior training. This suggests an important role for the lower brain stem and spinal cord in generating an appropriate strategy to maintain stability.

Heterogenic feedback between hindlimb extensors in the spontaneously locomoting premammillary cat.

Electrophysiological studies in anesthetized animals have revealed that pathways carrying force information from Golgi tendon organs in antigravity muscles mediate widespread inhibition among other antigravity muscles in the feline hindlimb. More recent evidence in paralyzed or nonparalyzed decerebrate cats has shown that some inhibitory pathways are suppressed and separate excitatory pathways from Golgi tendon organ afferents are opened on the transition from steady force production to locomotor activity. To obtain additional insight into the functions of these pathways during locomotion, we investigated the distribution of force-dependent inhibition and excitation during spontaneous locomotion and during constant force exertion in the premammillary decerebrate cat. We used four servo-controlled stretching devices to apply controlled stretches in various combinations to the gastrocnemius muscles (G), plantaris muscle (PLAN), flexor hallucis longus muscle (FHL), and quadriceps muscles (QUADS) during treadmill stepping and the crossed-extension reflex (XER). We recorded the force responses from the same muscles and were therefore able to evaluate autogenic (intramuscular) and heterogenic (intermuscular) reflexes among this set of muscles. In previous studies using the intercollicular decerebrate cat, heterogenic inhibition among QUADS, G, FHL, and PLAN was bidirectional. During treadmill stepping, heterogenic feedback from QUADS onto G and G onto PLAN and FHL remained inhibitory and was force-dependent. However, heterogenic inhibition from PLAN and FHL onto G, and from G onto QUADS, was weaker than during the XER. We propose that pathways mediating heterogenic inhibition may remain inhibitory under some forms of locomotion on a level surface but that the strengths of these pathways change to result in a proximal to distal gradient of inhibition. The potential contributions of heterogenic inhibition to interjoint coordination and limb stability are discussed.

Control of torque direction by spinal pathways at the cat ankle joint

To study the biomechanics of the calcaneal ten-dons complex insertion onto the calcaneus, we measured torque-time trajectories exerted by the triceps surae and tibialis anterior muscles in eight unanesthetized decerebrate cats using a multi-axis force-moment sensor placed at the ankle joint. The ankle was constrained to an angle of 110° plantarflexion. Muscles were activated using crossed-extension (XER), flexion (FWR), and caudal cutaneous sural nerve (SNR) reflexes. Torque contributions of other muscles activated by these reflexes were eliminated by denervation or tenotomy. In two animals, minia-ture pressure transducers were implanted among tendon fibers from the lateral gastrocnemius (LG) muscle that insert straight into the calcaneus or among tendon fibers from the medial gastrocnemius (MG) that cross over and insert on the lateral aspect of calcaneus. Reflexively evoked torques had the following directions: FWR, dorsiflexion and adduction; SNR, plantarflexion and abduction; and XER, plantarflexion and modest abduction or adduction. The proportion of abduction torque to plantarflexion torque was always greater for SNR than XER; this difference was about 50% of the magnitude of abduction torque generated by tetanic stimulation of the peronei. During SNR, pressures were higher in regions of the calcaneal tendon originating from MG than regions originating from LG. Similarly, pressures within the MG portion of the calcaneal tendon were higher during SNR than during XER, although these two reflexes produced matched ankle plantarflexion forces. Selective tenotomies and electromyographic recordings further demonstrated that MG generated most of the torque in response to SNR, while soleus, LG, and MG all generated torques in response to XER. Previous studies have shown that interneurons processing afferent information from both XER and SNR differentially excite the MG and LG motoneuron pools. Further, our data demonstrate that forces produced by this differential activation are preserved throughout the calcaneal tendon. We conclude that selective activation of the gastrocnemei permits the animal to take advantage of the complex mechanical insertion of MG and LG at calcaneus and, specifically, to generate different torques at the ankle joint in response to different reflex activations.

Musculoskeletal Mechanics: A Foundation of Motor Physiology

The design of the musculoskeletal system has always been a major consideration in the interpretation of experiments on the motor system. However, as motor physiology progresses toward a more comprehensive picture of motor behaviour, the study of the musculoskeletal system has of necessity, and of interest, come to depend more and more on the quantitative methods of biomechanics. Biomechanical studies have led to new hypotheses about the design of the motor system and biomechanical considerations have provided important tests of existing hypotheses concerning the neural control of movement. These hypotheses include global issues such as redundancy and encoded variables as well as specific hypotheses such as Stiffness Regulation, Selective Recruitment and the concept of Flexor Reflex Afferents.

Neuromuscular strategies for the transitions between level and hill surfaces during walking

Despite continual fluctuations in walking surface properties, humans and animals smoothly transition between terrains in their natural surroundings. Walking transitions have the potential to influence dynamic balance in both the anterior–posterior and medial–lateral directions, thereby increasing fall risk and decreasing mobility. The goal of the current manuscript is to provide a review of the literature that pertains to the topic of surface slope transitions between level and hill surfaces, as well as report the recent findings of two experiments that focus on the neuromuscular strategies of surface slope transitions. Our results indicate that in anticipation of a change in surface slope, neuromuscular patterns during level walking prior to a hill are significantly different from the patterns during level walking without the future change in surface. Typically, the changes in muscle activity were due to co-contraction of opposing muscle groups and these changes correspond to modifications in head pitch. In addition, further experiments revealed that the neck proprioceptors may be an initial source of feedback for upcoming surface slope transitions. Together, these results illustrate that in order to safely traverse varying surfaces, transitions strides are functionally distinct from either level walking or hill walking independently.

Chapter 32 The Role of Musculoskeletal Mechanics in Motor Coordination

Publisher Summary Spinal cord physiologists have long appreciated the importance of the mechanical properties of the peripheral motor apparatus in the production of coordinated movement. They have contributed much to the literature on muscle physiology in general and, in particular, on those properties that are expressed during normal motor behavior. The study of muscle and limb mechanics has been carried out along several specific lines of research, including intrinsic mechanics of single muscle fibers and motor units and muscles, muscle architecture, biomechanics of the musculoskeletal system, and kinesiology. This chapter discusses a number of relevant key findings published between 1900 and 1980 that were discovered by researchers primarily interested in the spinal mechanisms of motor coordination. The chapter then focuses on the more specific subject of the properties of muscle that are dependent upon the history of activation and prior movements and the relevance of these properties for motor coordination. In the first half of the twentieth century, investigators of spinal mechanisms studied musculoskeletal organization in relationship to reflex circuits. Sherrington and his coworkers recognized that the antagonistic, synergistic, and antigravity actions of muscle were important factors in the organization of basic reflex circuits.

Muscle spindle responses to horizontal support surface perturbation in the anesthetized cat: insights into the role of autogenic feedback in whole body postural control

Intact cats and humans respond to support surface perturbations with broadly tuned, directionally sensitive muscle activation. These muscle responses are further sensitive to initial stance widths (distance between feet) and perturbation velocity. The sensory origins driving these responses are not known, and conflicting hypotheses are prevalent in the literature. We hypothesize that the direction-, stance-width-, and velocity-sensitive muscle response during support surface perturbations is driven largely by rapid autogenic proprioceptive pathways. The primary objective of this study was to obtain direct evidence for our hypothesis by establishing that muscle spindle receptors in the intact limb can provide appropriate information to drive the muscle response to whole body postural perturbations. Our second objective was to determine if spindle recordings from the intact limb generate the heightened sensitivity to small perturbations that has been reported in isolated muscle experiments. Maintenance of this heightened sensitivity would indicate that muscle spindles are highly proficient at detecting even small disturbances, suggesting they can provide efficient feedback about changing postural conditions. We performed intraaxonal recordings from muscle spindles in anesthetized cats during horizontal, hindlimb perturbations. We indeed found that muscle spindle afferents in the intact limb generate broadly tuned but directionally sensitive activation patterns. These afferents were also sensitive to initial stance widths and perturbation velocities. Finally, we found that afferents in the intact limb have heightened sensitivity to small perturbations. We conclude that muscle spindle afferents provide an array of important information about biomechanics and perturbation characteristics highlighting their potential importance in generating appropriate muscular response during a postural disturbance.

A technique for measuring the mechanical actions of heterogenic (intermuscular) reflexes in the decerebrate cat.

Two muscle pullers were used to study the natural mechanical actions of autogenic reflexes, which arise from muscle receptors and feed back to the muscle of origin, and heterogenic reflexes, which feed back to muscles other than the muscle of origin. In the study reported here, the reflexes associated with muscles which act about the ankle joint of the decerebrate cat were investigated. Actions of autogenic pathways were measured by imposing length changes on the muscle and recording the resulting changes in force and EMG (electromyogram). Actions of heterogenic reflexes for pairs of muscles were measured by imposing appropriate combinations of length changes on the muscle of origin and on the muscle receiving the heterogenic reflex. In some cases, length changes were applied in such a way as to mimic normal mechanical coupling to evaluate the physiological importance of the reflexes, while in other cases the tests departed from normal coupling to address questions about mechanisms of reflex action. It was found that several pairs of muscles could be studied in a single experiment so that supraspinal influences on the pattern of spinal reflex connectivity can be conveniently evaluated.

Recovery of proprioceptive feedback from nerve crush

Non‐Technical Summary  Regeneration of muscle nerves damaged by crush reconnects the peripheral limb of neural circuits that pass through the spinal cord, but the mechanisms underlying functional recovery remain uncertain. We examined the actions of natural muscle stretch that initiates muscle contraction, i.e. the stretch reflex, through a spinal circuit that aids in adjusting body movement and posture in response to destabilizing forces in the external environment. Stretch applied to muscles reinnervated by crushed nerves produced reflexive contraction that was more forceful than normal, despite yielding less than normal synaptic excitation to spinal motoneurons. Incomplete recovery of synaptic function by stretch‐activated sensory neurons means that the enhanced stretch reflex contraction necessarily involves additional neural adaptations, possibly increased motoneuron excitability. These findings give further support to the importance of the central nervous system in restoring the ability of the regenerated neuromuscular system to respond to external disturbances of movement and posture.