A stretch reflex in extraocular muscles of species purportedly lacking muscle spindles

It is generally assumed that proprioceptive feedback plays a crucial role in limb posture and movement. However, the role of afferent signals from extraocular muscles (EOM) in the control of eye movement has been a matter of continuous debate. These muscles have atypical sensory receptors in several species and it has been proposed that they are not supported by stretch reflexes. We recorded electromyographic activity of EOM during passive rotations of the eye in sedated rats and squirrel monkeys and observed typical stretch reflexes in these muscles. Results suggest that there is a similarity in the reflexive control of limb and eye movement, despite substantial differences in their biomechanics and sensory receptors. Like in some limb skeletal muscles, the stretch reflex in EOM in the investigated species might be mediated by other length-sensitive receptors, rather than muscle spindles.     

Changes in size of the stretch reflex of cat and man attributed to aftereffects in muscle spindles

1. This is a report of experiments carried out on the cat and on man, which demonstrate that conditioning of a muscle by contraction and movement can lead to changes in amplitude of stretch reflexes elicited in that muscle. 2. In triceps surae of the cat, the reflex response to a brief stretch was recorded after conditioning with a whole-muscle contraction followed by a pause at a length either 5 mm longer or shorter than the length at which the reflex was elicited. Following conditioning at the long length the reflex response was less than half as large as that following conditioning at the short length. 3. The changes in reflex amplitude could be correlated with an altered stretch responsiveness of muscle spindles in the soleus muscle. When the muscle had been held long during conditioning, a subsequent brief stretch applied at an intermediate length elicited fewer impulses in primary endings of spindles than after conditioning at a short length. 4. The same kind of experiment was then carried out on adult human subjects. When a tendon tap was applied to the Achilles tendon after a voluntary contraction and relaxation of triceps surae with the muscle at a long length, (foot dorsiflexed) the reflex was frequently less than half the size it had been after a contraction at a short length (foot plantarflexed). It was concluded that the same kind of spindle aftereffects as observed for cat soleus spindles were responsible for the changes in reflex amplitude. 5. It was found both in the cat and in human subjects that the changes in reflex amplitude after conditioning became progressively less as the test length was made longer. 6. The explanation put forward to account for these observations is that stable cross-bridges form between actin and myosin filaments of passive intrafusal (and extrafusal) fibers. When the muscle is shortened several seconds after a contraction at a long length, the intrafusal fibers, stiffened by the presence of cross-bridges, fall slack. Slack does not develop after a contraction at a short muscle length, as the fiber is stretched to the test length. Since any slack must first be taken up by the test stretch, there is a smaller afferent response and consequently a smaller reflex contraction in response to a tendon tap after conditioning at a long length.(ABSTRACT TRUNCATED AT 400 WORDS)     

The responses of muscle spindles in the kitten to stretch and vibration

Summary Discharges of muscle spindle afferents from the soleus muscle were studied in kittens aged 1–21 days and in adult cats. Vibration applied longitudinally to the tendon elicited one impulse for each cycle of vibration over the range 1–200 Hz for the kittens and up to 450 Hz for the adult. Threshold amplitudes were generally higher in the kitten than in the adult. In response to large ramp and hold stretches applied at long muscle lengths kitten spindles showed rate saturation during the length change. Dynamic index, that is the peak rate during the length change minus the rate at the final length became progressively smaller at longer muscle lengths. No sign of saturation was seen at comparable muscle lengths in the adult. It is suggested that in the newborn the bag₁ intrafusal fibre is not functional and that the dynamic response is produced only by the afferent terminals on the bag₂ fibre. Another difference between kitten and adult was the length sensitivity measured under dynamic conditions. This increased much more steeply with stretch rate in the kitten. One possible explanation for the higher dynamic length sensitivity is a lack of elastic fibres surrounding intrafusal fibres of immature spindles.     

The response to stretch of human intercostal muscle spindles studied in vitro.

1. The discharge properties of human muscle spindles have been studied in vitro in a preparation based on the biopsied external intercostal muscle. 2. The static and dynamic responsiveness of thirty-six endings in twenty visualized and histologically identified spindles have been investigated using amplitudes and velocities of stretch likely to encompass those occurring in vivo. 3. The dynamic index, measured at a stretch velocity of 3 mm/sec, ranged from 3 to 40 impulses/sec and was distributed bimodally, consitent with the presence of primary and secondary endings. 4. The relationship between the dynamic index and the velocity of stretch was approximately linear both for primary and secondary endings up to the maximum velocity tested (10 mm/sec). 5. The frequency/extension relationship was approximately linear for both primary and secondary endings. The mean values of the slope for primary and secondary endings were 16-1 +/- 8-3 S.D. of the observation and 12-1 +/- 6-5 impulses/sec per five per cent extension. 6. The slopes of the frequency/extension relationship for endings lying in the same spindle were positively correlated, significant at the 10% level. 7. It was estimated from the results in vitro that the position sensitivity of human intercostal spindles in vivo ranges from 2 to 21 impulses/sec per millimetre.     

Adaptation of the discharge of frog muscle spindles following a stretch

1. Stretching a frog muscle spindle evoked a discharge of action potentials in its sensory axon. As the rate of this discharge decreased during the adaptation that followed the dynamic phase of a stretch, the variability of the interspike intervals of the impulse train increased.2. Adaptation occurred in two phases. At first the impulse train was almost regular and adapted rapidly, but later this gave way to a phase of slower adaptation where the variability of the discharge was much increased. In the second phase of adaptation the interspike intervals increased in length less than half as quickly as in the first phase.3. When the rate of adaptation changed from the more rapid to the slower phase there was often an abrupt change in the character of the discharge and the relationship between the mean interspike interval and the variability changed. The interspike interval at which this change-over occurred was relatively constant in records of the discharge from one afferent fibre even though stretches of different amplitude were employed, though it differed from one afferent fibre to another.4. These features of the discharge during adaptation suggest that the two sections of the impulse trains were derived from different spike generators by a process of probabilistic mixing.     

Enhanced stretch reflex excitability of the soleus muscle in experienced swimmers

The purpose of this study was to investigate effects of long-term participation to swimming on adaptations of spinal reflex excitability. To this end, mechanically induced stretch reflex (SR) and electrically induced Hoffmann (H-) reflex of the soleus muscle were investigated between swimmers with experience of more than 10 years and non-trained individuals while sitting at rest. The amplitude and the gain (stretch velocity vs. amplitude of the reflex response) of the SR were significantly greater in the swimming group than in the non-trained control group. Similarly, the responses of the H-reflex were also significantly greater in the swimming group than in the non-trained control group. Results of this study demonstrated that the spinal reflex excitability in experienced swimmers was far more enhanced than in non-trained individuals.     

Intramuscular localization of monosynaptic Ia reflex effects in the cat biceps femoris muscle

Intracellular recordings from biceps femoris (BF) motoneurons were made in anesthetized low spinal cats during periods of electrical stimulation of the nerve branches supplying the anterior, middle and posterior portions of the BF muscle and the nerves to semimembranosus and semitendinosus. Measurements were made of each cell's composite intrahomonymous and heteronymous monosynaptic Ia-EPSP responses to stimulation of the test nerves (branches). We have found evidence for an intramuscular localization of these monosynaptic Ia reflex effects not only when comparing responses between the two functional components of the BF muscle as is well established [6] but, in addition, when comparing responses between different parts of each functional (hip extensor and knee flexor) component as well. It is argued that both somatotopic and neuronal recognition factors may contribute to the localization of these monosynaptic reflex effects.     

Long-latency component of the stretch reflex in human muscle is not mediated by intramuscular stretch receptors

Reflex responses to mechanical stimulation of muscle (brief imposed movement) were investigated. Reflexes were elicited in the forefinger, recording from the first dorsal interosseous (FDI), and in the foot, recording from soleus. These responses typically consisted of a short-latency component (M1) and a long-latency component (M2) at 33 ms and 53 ms, respectively, after the stimulus in the case of FDI, and 37 ms and 68 ms, respectively, in soleus upon stimulation of the sole of the foot. Normally, when a muscle is stretched by a mechanical stimulus (either naturally or by an experimentally imposed movement), both skin receptors and muscle stretch receptors are activated. It is possible, however, to devise stimulation parameters where this is not the case. Fixating the finger with plasticine enables the effects of skin stimulation to be studied without stretching the FDI muscle. On the other hand, tapping a long tendon allows muscle stretch receptors to be activated without involving skin or subcutaneous structures. Component M1 was always abolished by finger fixation in 40 trials on 10 subjects, with M2 being essentially unchanged in latency, duration, or amplitude. Reflex responses were obtained in soleus muscle in nine experiments by prodding the sole of the foot (thereby stimulating both skin and muscle stretch receptors). Alternatively, the tendo achilles was prodded (which solely activates stretch receptors in the muscle). In the former, M1 and M2 were generated. In the latter, only M1 was produced. It is concluded that the long-latency component of the stretch reflex, M2, originates in skin and/or subcutaneous nerve terminals and that no part of M2 originates in muscle stretch receptors.     

The effects of experimental muscle and skin pain on the static stretch sensitivity of human muscle spindles in relaxed leg muscles

Animal studies have shown that noxious inputs onto γ-motoneurons can cause an increase in the activity of muscle spindles, and it has been proposed that this causes a fusimotor-driven increase in muscle stiffness that is believed to underlie many chronic pain syndromes. To test whether experimental pain also acts on the fusimotor system in humans, unitary recordings were made from 19 spindle afferents (12 Ia, 7 II) located in the ankle and toe extensors or peronei muscles of awake human subjects. Muscle pain was induced by bolus intramuscular injection of 0.5 ml 5% hypertonic saline into tibialis anterior (TA); skin pain was induced by 0.2 ml injection into the overlying skin. Changes in fusimotor drive to the muscle spindles were inferred from changes in the mean discharge frequency and discharge variability of spindle endings in relaxed muscle. During muscle pain no afferents increased their discharge activity: seven afferents (5 Ia, 2 II) showed a decrease and six (4 Ia, 2 II) afferents were not affected. During skin pain of 13 afferents discharge rate increased in one (Ia) and decreased in two (1 Ia, 1 II). On average, the overall discharge rate decreased during muscle pain by 6.1% ( P < 0.05; Wilcoxon), but remained essentially the same during skin pain. There was no detectable correlation between subjective pain level and the small change in discharge rate of muscle spindles. Irrespective of the type of pain, discharge variability parameters were not influenced ( P > 0.05; Wilcoxon). We conclude that, contrary to the 'vicious cycle' hypothesis, acute activation of muscle or skin nociceptors does not cause a reflex increase in fusimotor drive in humans. Rather, our results are more aligned with the pain adaptation model, based on clinical studies predicting pain-induced reductions of agonist muscle activity.     

Tissue engineering the monosynaptic circuit of the stretch reflex arc with co-culture of embryonic motoneurons and proprioceptive sensory neurons

The sensory circuit of the stretch reflex arc is composed of intrafusal muscle fibers and their innervating proprioceptive neurons that convert mechanical information regarding muscle length and tension into action potentials that synapse onto the homonymous motoneurons in the ventral spinal cord which innervate the extrafusal fibers of the same muscle. To date, the in?vitro synaptic connection between proprioceptive sensory neurons and spinal motoneurons has not been demonstrated. A functional in?vitro system demonstrating this connection would enable the understanding of feedback by the integration of sensory input into the spinal reflex arc. Here we report a co-culture of rat embryonic motoneurons and proprioceptive sensory neurons from dorsal root ganglia (DRG) in a defined serum-free medium on a synthetic silane substrate (DETA). Furthermore, we have demonstrated functional synapse formation in the co-culture by immunocytochemistry and electrophysiological analysis. This work will be valuable for enabling in?vitro model systems for the study of spinal motor control and related pathologies such as spinal cord injury, muscular dystrophy and spasticity by improving our understanding of the integration of the mechanosensitive feedback mechanism.     

Evidence that the secondary as well as the primary endings of the muscle spindles may be responsible for the tonic stretch reflex of the decerebrate cat

1. The size of the tonic stretch reflex of the soleus or gastrocnemius muscle of the decerebrate cat has been compared with the size of the reflex contraction elicited in the same muscle by high-frequency vibration applied to its tendon.2. On the assumption that vibration preferentially excites the primary endings of the muscle spindles it may be used to estimate the relation between the reflex response and the frequency of the Ia input to the spinal cord. On this basis, the increase in tension evoked by increasing extension is too great to be explained by the increase in Ia input with extension previously found on single fibre recording in comparable preparations.3. When vibration was superimposed on stretch reflexes elicited by different extensions, the size of the additional contraction elicited by the vibration remained approximately constant. If the stretch and vibration reflexes both depended entirely upon the Ia pathway, then occlusion between them would have been expected instead of the simple summation which was found.4. The absence of occlusion was not due to variation of the contractile strength of the muscle with its extension. This was shown by finding that the reflex contraction of soleus produced by stimulating the medial gastrocnemius nerve also remained the same size when elicited at different lengths of the muscle.5. The reflex effects were studied of superimposing alternate stretches and releases of 0.2 mm, on extensions of several mm. The small stretches elicited responses which were larger than expected from the response to large stretches, and which were approximately the same size at different mean lengths of the muscle.6. It is concluded that the tonic stretch reflex of the decerebrate cat cannot readily be explained solely by the increase in Ia discharge produced by stretching, as usually believed. Instead, it is suggested that the group II afferent fibres from the secondary endings of the muscle spindle also play an important part in its production.     

Role of nerve and muscle factors in the development of rat muscle spindles

The soleus muscles of fetal rats were examined by electron microscopy to determine whether the early differentiation of muscle spindles is dependent upon sensory innervation, motor innervation, or both. Simple unencapsulated afferent-muscle contacts were observed on the primary myotubes at 17 and 18 days of gestation. Spindles, encapsulations of muscle fibers innervated by afferents, could be recognized early on day 18 of gestation. The full complement of spindles in the soleus muscle was present at day 19, in the region of the neuromuscular hilum. More afferents innervated spindles at days 18 and 19 of gestation than at subsequent developmental stages, or in adult rats; hence, competition for available myotubes may exist among afferents early in development. Some of the myotubes that gave rise to the first intrafusal (bag₂) fiber had been innervated by skeletomotor (α) axons prior to their incorporation into spindles. However, encapsulated intrafusal fibers received no motor innervation until fusimotor (γ) axons innervated spindles 3 days after the arrival of afferents and formation of spindles, at day 20. The second (bag₁) intrafusal fiber was already formed when γ axons arrived. Thus, the assembly of bag₁ and bag₂ intrafusal fibers occurs in the presence of sensory but not γ motor innervation. However, transient innervation of future bag₂ fibers by α axons suggests that both sensory and α motor neurons may influence the initial stages of bag₂ fiber assembly. The confinement of nascent spindles to a localized region of the developing muscle and the limited number of spindles in developing muscles in spite of an abundance of afferents raise the possibility that afferents interact with a special population of undifferentiated myotubes to form intrafusal fibers.     

The role of joint biomechanics in determining stretch reflex latency at the normal human ankle

Summary In order to study the influence of biomechanical factors on the timing of stretch reflex activity in the ankle extensor musculature, well defined, small amplitude and relatively rapid dorsiflexing stretch was applied to the ankle of seated normal human subjects at a series of angles within the range of physiological movement. If the ankle musculature was relaxed, a single reflex component appeared in the Triceps surae (TS) EMG with a latency compatible with a predominantly monosynaptic pathway. The latency of this response could be prolonged by applying stretch from an initially plantarflexed position and, similarly, decreased by applying stretch from a dorsiflexed position. A decrease in latency of 5–30 ms could be achieved by altering the pre-displacement ankle angle from 105 to 75 degrees. Intermediate changes in the start angle led to intermediate changes in latency. This trend was highly linear. If stretch was applied while the subject maintained a low level contraction in the TS, however, this shift in latency was abolished, with the earliest reflex components appearing with a latency obtained in the relaxed state at or close to maximum dorsiflexion. It is suggested that this shift in latency results from the properties of the long, compliant tendon through which joint movements are transmitted to the TS muscle. This shift in latency caused by passive alteration in the ankle angle at which a reflex was evoked should be taken into account when classifying reflexes arising from a mechanical input, or when using latency determinations as evidence for the involvement of particular pathways in their genesis.