Contribution of force feedback to ankle extensor activity in decerebrate walking cats

Previous investigations have demonstrated that feedback from ankle extensor group Ib afferents, arising from force-sensitive Golgi tendon organs, contributes to ankle extensor activity during the stance phase of walking in the cat. The objective of this investigation was to gain insight into the magnitude of this contribution by determining the loop gain of the positive force feedback pathway. Loop gain is the relative contribution of force feedback to total muscle activity and force. In decerebrate cats, the isolated medial gastrocnemius muscle (MG) was held at different lengths during sequences of rhythmic contractions associated with walking in the other three legs. We found that MG muscle activity and force increased at longer muscle lengths. A number of observations indicated that this length dependence was not due to feedback from muscle spindles. In particular, activity in group Ia afferents was insensitive to changes in muscle length during the MG bursts, and electrical stimulation of group II afferents had no influence on the magnitude of burst activity in other ankle extensors. We concluded that the homonymous positive force feedback pathway was isolated from other afferent pathways, allowing the use of a simple model of the neuromuscular system to estimate the pathway loop gain. This gain ranged from 0.2 at short muscle lengths to 0.5 at longer muscle lengths, demonstrating that force feedback was of modest importance at short muscle lengths, accounting for 20% of total activity and force, and of substantial importance at long muscle lengths, accounting for 50%. This length dependence was due to the intrinsic force-length property of muscle. The gain of the pathway that converts muscle force to motoneuron depolarization was independent of length. We discuss the relevance of this conclusion to the generation of ankle extensor activity in intact walking cats. These findings emphasize the general importance of feedback in generating ankle extensor activity during walking in the cat.     

Head pitch affects muscle activity in the decerebrate cat hindlimb during walking

Our purpose was to quantify the effects of head pitch on muscle activity patterns of the decerebrate cat hindlimb during walking. Five decerebrate cats walked at 0.7 m/s on a treadmill positioned level with the head pitch either parallel to the treadmill, 50% nose down or 50% nose up. We collected electromyography data from six hindlimb muscles. During level walking, after we manipulated head pitch, our results were surprisingly equivalent to the research on slope walking. For instance, muscle activity during level walking with a 50% head pitch nose down mimicked uphill walking. The muscle activity of the iliopsoas and semitendinosus significantly increased. Muscle activity during level walking with a 50% head pitch nose up mimicked downhill walking. Specifically, the biceps femoris and semimembranosus were inactive during the entire step. These alterations in muscle activity occurred within one step of altering head pitch but dissipated as level walking continued. In conclusion, the time course of muscle activity patterns due to modifications in head pitch is immediate and transitory.     

Comparison of the effects of stimulating extensor group I afferents on cycle period during walking in conscious and decerebrate cats

Previous studies have reported that stimulation of group I afferents from extensor muscles prolongs stance duration during walking in decerebrate cats. The main objective of this investigation was to determine whether this phenomenon occurs during walking in conscious cats. In conscious cats without lesions of the central nervous system (CNS), stimulation of group I afferents in the lateral gastrocnemius/soleus (LGS) nerve during stance prolonged extensor burst duration and increased the cycle period in five of seven animals. The mean increases in cycle period were modest, ranging from 6 to 22%. In five of six animals that walked both quadrupedally and bipedally at the same rate, the effects on cycle period were stronger during bipedal stepping (18% mean increase in cycle period compared with 9%). The stimulated nerves were transected and the experimental procedure was usually delayed in the conscious animals for 2–3 days following implantation of the stimulating electrodes. To assess whether chronic axotomy of the LGS nerve was a factor in the decreased effectiveness, four of the cats with chronic nerve section were decerebrated and their LGS nerves were stimulated after the animals began to spontaneously walk on a motorized treadmill. In all four of these animals, the effects of stimulating the chronically cut LGS nerve on the step cycle period became stronger following decerebration. However, these effects were not as strong as those produced when an acutely sectioned LGS nerve was stimulated. During both quadrupedal and bipedal walking, stimulation of the LGS nerve increased the amplitude of the medial gastrocnemius (MG) electromyogram. The augmented activity of the MG muscle contributed to an increased extension of the ankle during stimulated steps. The conclusion from these experiments is that stimulation of the group I afferents in extensor nerves can prolong stance in the conscious cat, but this effect is weaker than in decerebrate animals. It is likely that transmission in the polysynaptic group I pathways controlling stance duration is regulated in a complex fashion by descending signals from the brain in the conscious animal. Received: 6 December 1996 / Accepted: 4 June 1997     

Contribution of afferent feedback to the soleus muscle activity during human locomotion

During the stance phase of the human step cycle, the ankle undergoes a natural dorsiflexion that stretches the soleus muscle. The afferent feedback resulting from this stretch enhances the locomotor drive. In this study a robotic actuator was used to slightly enhance or reduce the natural ankle dorsiflexion, in essence, mimicking the small variations in the ankle dorsiflexion movement that take place during the stance phase of the step cycle. The soleus (SOL) and tibialis anterior EMG were analyzed in response to the ankle trajectory modifications. The dorsiflexion enhancements and reductions generated gradual increments and decrements, respectively, in the ongoing SOL EMG. We exercised care to ensure that the imposed ankle movements were too slow to elicit distinct burst-like stretch reflex responses that have been investigated previously. The increased SOL EMG after the dorsiflexion enhancements was reduced when the group Ia afferents were blocked with peripheral ischemia at the thigh, and during high-frequency Achilles tendon vibration. However, neither ischemia nor tendon vibration affected the decrements in the SOL EMG during the dorsiflexion reductions. These findings give evidence of the contribution of afferent feedback to the SOL activity in an ongoing basis during the stance phase. The results suggest that mainly feedback from the group Ia pathways is responsible for the increments in the SOL EMG during the dorsiflexion enhancements. However, the decrements in the SOL activity might be mediated by different afferent mechanisms.     

Sartorius muscle afferents influence the amplitude and timing of flexor activity in walking decerebrate cats

Recent investigations have demonstrated that afferent signals from hindlimb flexor muscles can strongly influence flexor burst activity during walking and during fictive locomotion in decerebrate cats. We have reported previously that modifying afferent feedback from the sartorius (Sart) muscles by assisting or resisting hip flexion has a marked effect on the magnitude and duration of activity in iliopsoas (IP) as well as the sartorius muscles. The objective of the present investigation was to identify the afferents responsible for these effects by examining, in walking decerebrate cats, the influence of electrically stimulating sartorius afferents on burst activity in the IP and tibialis anterior (TA) muscles. Stimulation of the sartorius nerve at group I strength resulted in an increase in the duration of IP and TA bursts and an increase in the magnitude of IP bursts. The effect on burst durations was only observed at stimulus strengths of 1.6 T and higher. At lower stimulus strengths, there was a strong excitatory effect on IP bursts but no effect on TA bursts. Stimulation of the sartorius nerve at group II strength yielded variable results. When group II stimulation was delivered repeatedly during a walking sequence, the initial response was usually a strong inhibition of burst activity in IP and TA followed by a progressive reduction in inhibition and the emergence in IP of an excitatory response. This observation, together with findings of previous studies, suggests the existence of parallel excitatory and inhibitory pathways from sartorius group II afferents to flexor motoneurons. Taken together, these results support an earlier speculation that feedback from large afferents from the sartorius muscles has a strong influence on the generation of flexor burst activity in walking cats. Electronic Publication     

Contribution of peripheral afferents to the activation of the soleus muscle during walking in humans

Summary Small, rapid stretches were applied to the soleus muscle during the stance phase of walking by lifting the forefoot with a pneumatic device. Stretch responses were induced in the soleus muscle by the disturbance. The amplitude and time course of the responses from the soleus muscle were a function of both the kinematics of the disturbance and the time in the step cycle when the disturbance was applied. The step cycle was divided into 16 equal time parts, and data obtained within each of these parts were averaged together. The electromyographic (EMG) response of the soleus muscle showed a time course that was similar to the time course of the angular velocity induced by the disturbance at the ankle. Three linear equations were used to predict the EMG response from the soleus muscle as a function of the angular kinematics of the disturbance: 1) velocity, 2) velocity and displacement, 3) velocity, displacement and acceleration. Introduction of a pure delay between the EMG and the kinematics substantially improved the predictions. Most of the variance (70%) in the EMG response could be accounted for by the velocity of the disturbance alone with an optimal delay (average 38 ms). Inclusion of a displacement term significantly increased the variance accounted for (85%), but further addition of an acceleration term did not. Since the velocity of the disturbance accounted for most of the variance, the reflex gain was estimated from the velocity coefficient. This coefficient increased in a ramp-like fashion through the early part of the stance phase, qualitatively similar to the increase in the H-reflex. Based on these identified gains, this reflex pathway was estimated to contribute substantially (30% to 60%) to the activation of the soleus muscle particularly during the early part of the stance phase.     

Muscle activity during forelimb stepping in decerebrate cats.

In decerebrate cats with the lower thoracic cord transected, electromyographic activities were analyzed in up to 41 forelimb muscles, almost all muscles involved in forelimb stepping (intrinsic hand muscles were not included). From the active period in the step cycle, muscles were classified into three groups: extensors, of which activity is like that of elbow extensors; flexors, activity like that of elbow flexors; others, including dorsiflexors of the wrist, pronators, and supinator. The results were well consistent with those from conscious animals as well as efferent pattern of fictive locomotion in elbow and distal muscles. Nevertheless, in some proximal muscles discrepancies were noted, suggesting their changeability depending on environmental conditions. Recording from almost all muscles allowed to estimate rhythmic change of the overall output of the forelimb central pattern generator.     

Resetting of resultant stiffness in ankle flexor and extensor muscles in the decerebrate cat

Summary Flexor (tibialis anterior, TA, and extensor digitorum longus, EDL) and extensor (soleus, SOL) muscles in the decerebrate cat were subjected to length changes and the force responses were measured. Resultant muscular stiffness, which arises from the mechanical reaction of muscle fibers contracting prior to the length change and from a change in force due to reflex action, was calculated by dividing the changes in force by the corresponding length changes. As shown previously in the premammillary preparation, resultant stiffness was usually higher in SOL than in TA or EDL. Following an intercollicular transection in some preparations, resultant stiffness increased markedly for TA but not substantially for SOL. During continuous electrical stimulation in the magnocellular red nucleus in premammillary preparations, resultant stiffness of SOL decreased for a wide range of forces while EDL responses were unaffected. These results show that reflex gain is not determined solely by the level of motoneuronal excitability but also by a descending control from the brainstem, and that the lower resultant stiffness in flexors compared to extensors in the decerebrate cat is set by this control system and not by inherent differences in the strength of autogenetic reflex pathways for the two muscles.     

Use of galvanic vestibular feedback to control postural orientation in decerebrate rabbits

In quadrupeds, the dorsal-side-up body orientation during standing is maintained due to a postural system that is driven by feedback signals coming mainly from limb mechanoreceptors. In caudally decerebrated (postmammillary) rabbits, the efficacy of this system is considerably reduced. In this paper, we report that the efficacy of postural control in these animals can be restored with galvanic vestibular stimulation (GVS) applied transcutaneously to the labyrinths. In standing intact rabbits, GVS causes a lateral body sway towards the positive electrode. We used this GVS-caused sway to counteract the lateral body sway resulting from a mechanical perturbation of posture. Experiments were performed on postmammillary rabbits that stood on the tilting platform with their hindlimbs. To make the GVS value dependent on the postural perturbation (i.e., on the lateral body sway caused by tilt of the platform), an artificial feedback loop was formed in the following ways: 1) Information about the body sway was provided by a mechanical sensor; 2) The GVS current was applied when the sway exceeded a threshold value; the polarity of the current was determined by the sway direction. This simple algorithm allowed the "hybrid" postural system to maintain the dorsal-side-up orientation of the hindquarters when the platform was tilted by ± 20°. Thus, an important postural function, i.e., securing lateral stability during standing, can be restored in decerebrate rabbits with the GVS-based artificial feedback. We suggest that such a control system can compensate for the loss of lateral stability of various etiologies, and can be used for restoration of balance control in patients with impaired postural functions.     

Alterations in simple spike activity and locomotor behavior associated with climbing fiber input to Purkinje cells in a decerebrate walking cat

Recently we reported significant modulation of climbing fiber discharge in cerebellar Purkinje cells during normal and perturbed locomotion in the decerebrate cat walking on a treadmill. In this study covariation of simple spike activity and step cycle behavior with complex spike discharge were studied in decerebrate cats. Purkinje cell simple and complex spike discharge was recorded extracellularly in the intermediate region of lobules IV and V. Forelimb triceps and biceps electromyographic activity and displacement were monitored during the step cycle. A series of analyses were carried out to determine the temporal relationship between the complex spike discharge and forelimb step cycle, electromyographic activity and simple spike discharge. In this paper only the complex spike discharge associated with the onset of locomotion was evaluated. Using a sorting technique the amplitude of the forelimb step cycle and the associated triceps and biceps electromyographic activity covaried with complex spike discharge. For the majority of cells the alterations in the step cycle followed or occurred with the increase in complex spike discharge. However, in some cells the step cycle modifications preceded the increase in climbing fiber afferent activity. Another series of analyses employing an alignment technique demonstrated that a short term increase in simple spike discharge followed and was tightly coupled to the complex spike discharge. Additionally in most Purkinje cells an "oscillation" of simple spike activity which followed the complex spike discharge was uncovered. These observations support an important role for the climbing fiber afferent system in ongoing motor behavior. The results are consistent with the speculation that increased climbing fiber afferent input alters cerebellar cortical output which in turn can alter the ongoing motor behavior.     

Modulation of motor patterns by sensory feedback during earthworm locomotion

Role of sensory feedback to motor pattern activity concerning locomotion in the earthworm, Eisenia fetida, was investigated. We have previously reported that bath application of octopamine induces fictive locomotion in the earthworm. In this study, we have examined the role of sensory feedback during fictive locomotion by analyzing electrical activities from the cut end and intact first lateral nerves of the ventral nerve cord (VNC). From the cut end recordings, motor activity associated with fictive locomotion was measured. A mixture of sensory and motor activities was measured from the intact first lateral nerve using en passant recordings, and sensory activity was separated by subtraction of the cut end recording (mainly motor activities) from the intact first lateral nerve recording. We estimated the effect of sensory feedback from the earthworm body wall by comparing recordings that made when the preparation was in-contact with a substrate or suspended above it. Motor pattern activities and the coefficient of variation for inter-spike-interval of motor outputs were increased under suspended conditions during circular muscle contraction. These results indicate that sensory feedback modulates the pattern of motor activity in the earthworm during locomotion.     

Responses of Renshaw cells coupled with hindlimb extensor motoneurons to sinusoidal stimulation of labyrinth receptors in the decerebrate cat

Contraction of ipsilateral limb extensors during side-down roll tilt of the head, leading to selective stimulation of labyrinth receptors, is attributed to an increased discharge of excitatory vestibulospinal (VS) neurons (alpha-responses) and a decreased discharge of medullary inhibitory reticulospinal (RS) neurons (beta-responses), both of which act on ipsilateral extensor motoneurons. Experiments were performed in decerebrate cats, with the de-efferented gastrocnemius-soleus (GS) muscle fixed at a constant length, to find out whether Renshaw (R) cells linked with GS motoneurons responded to labyrinth stimulation elicited by head rotation, while the neck had been bilaterally deafferented. We hoped in this way to clarify the role and the mechanism by which these inhibitory interneurons act on limb extensor motoneurons during the vestibular reflexes. 72.7% of the R-cells, disynaptically excited by group I volleys elicited by single shock stimulation of the GS nerve, weakly responded to head rotation at frequencies of 0.026-0.15 Hz and at a peak amplitude of 10 degrees. For the frequency of head rotation of 0.026 Hz, +/- 10 degrees C, most of the GS R-cells increased their firing rate during side-down head displacement (alpha-responses); some responses were related to head position, but others showed some phase lead or lag with respect to head position. The gain of the first harmonic of these unit responses was very low and corresponded on the average to 0.084 +/- 0.062, S.D. imp./s/deg, while the sensitivity corresponded to 2.14 +/- 2.35, S.D.%/deg (base frequency, 6.85 +/- 5.97, S.D. imp./s). These responses were attributed to the activity of VS neurons, the increased discharge of which during side-down head rotation exerts a weak excitatory influence on a limited number of GS motoneurons and, through their recurrent collaterals, on the related R-cells. The modulation of the firing rate of R-cells coupled with the GS motoneurons increased linearly by increasing the peak amplitude of displacement from 5 degrees to 20 degrees at the frequency of 0.026 Hz, so that the response gain remained almost unchanged. An increase in frequency of head rotation from 0.026 to 0.32 Hz at a fixed amplitude of 10 degrees, thus changing the maximal angular acceleration from 0.26 degrees/s2 to 41.7 degrees/s2, reversed the response pattern of R-cells reported above. The resulting beta-responses, which also showed some phase lead or lag with respect to head position, were attributed to vestibular activation of RS neurons.(ABSTRACT TRUNCATED AT 400 WORDS)