Intercostal Muscle Spindles Research Articles

Analysis of activity of motor units in the biceps brachii muscle after intercostal-musculocutaneous nerve transfer

We examined respiratory activity of motor units (MUs) in the internal intercostal nerves (IICNs)-transferred biceps brachii muscle (IC-biceps) in cats. MUs of IC-biceps showed respiratory discharges in inspiratory and expiratory phases, and these were enhanced by CO 2 inhalation. Narrowing the airway also enhanced inspiratory and expiratory MUs activity. A mechanical load to the thorax immediately enhanced inspiratory MUs activity and weakened expiratory MUs activity. We analyzed the cross-correlation of MUs activity in interchondral muscle and IC-biceps to characterize the respiratory spinal descending inputs to motoneurons. We confirmed the short-term synchronization from interchondral muscles indicating divergence of a single respiratory presynaptic axon to thoracic motoneurons, but could not find synchronization from IC-biceps. The motor axonal conduction velocity (axonal CV) of IC-biceps MUs was lower than that of interchondral muscles. There was no correlation between the respiratory recruitment order of IC-biceps MUs and their axonal CV. These results indicate that IC-biceps shows the respiratory activities and afferent inputs from intercostal muscle spindles in the neighboring segments remain influential on activity of IC-biceps. In addition, the short-term synchronization from IC-biceps could not be found, suggesting that the intercostal nerve transfer alters the respiratory spinal descending inputs to thoracic motoneurons.

Mechanical effect of muscle spindles in the canine external intercostal muscles

High-frequency mechanical vibration of the ribcage increases afferent activity from external intercostal muscle spindles, but the effect of this procedure on the mechanical behaviour of the respiratory system is unknown. In the present study, we have measured the changes in external intercostal muscle length and the craniocaudal displacement of the ribs during ribcage vibration (40 Hz) in anaesthetized dogs. With vibration, external intercostal inspiratory activity increased by approximately 50 %, but the respiratory changes in muscle length and rib displacement were unaltered. A similar response was obtained after the muscles in the caudal segments of the ribcage were sectioned and the caudally oriented force exerted by these muscles on the rib was removed, thus suggesting that activation of external intercostal muscle spindles by vibration generates little tension. Prompted by this observation, we also examined the role played by the external intercostal muscle spindles in determining the respiratory displacement of the ribs during breathing against high inspiratory airflow resistances. Although resistances consistently elicited prominent reflex increases in external intercostal inspiratory activity, the normal inspiratory cranial displacement of the ribs was reversed into an inspiratory caudal displacement. Also, this caudal rib displacement was essentially unchanged after section of the external intercostal muscles, whereas it was clearly enhanced after denervation of the parasternal intercostals. These findings indicate that stretch reflexes in external intercostal muscles confer insufficient tension on the muscles to significantly modify the mechanical behaviour of the respiratory system.

Mechanical effect of muscle spindles in the canine external intercostal muscles.

High-frequency mechanical vibration of the ribcage increases afferent activity from external intercostal muscle spindles, but the effect of this procedure on the mechanical behaviour of the respiratory system is unknown. In the present study, we have measured the changes in external intercostal muscle length and the craniocaudal displacement of the ribs during ribcage vibration (40 Hz) in anaesthetized dogs. With vibration, external intercostal inspiratory activity increased by approximately 50 %, but the respiratory changes in muscle length and rib displacement were unaltered. A similar response was obtained after the muscles in the caudal segments of the ribcage were sectioned and the caudally oriented force exerted by these muscles on the rib was removed, thus suggesting that activation of external intercostal muscle spindles by vibration generates little tension. Prompted by this observation, we also examined the role played by the external intercostal muscle spindles in determining the respiratory displacement of the ribs during breathing against high inspiratory airflow resistances. Although resistances consistently elicited prominent reflex increases in external intercostal inspiratory activity, the normal inspiratory cranial displacement of the ribs was reversed into an inspiratory caudal displacement. Also, this caudal rib displacement was essentially unchanged after section of the external intercostal muscles, whereas it was clearly enhanced after denervation of the parasternal intercostals. These findings indicate that stretch reflexes in external intercostal muscles confer insufficient tension on the muscles to significantly modify the mechanical behaviour of the respiratory system.

Response of the canine internal intercostal muscles to chest wall vibration.

Although high-frequency mechanical vibration of the rib cage reduces dyspnea, its effects on the respiratory muscles are largely unknown. We have previously shown that in anesthetized dogs, vibrating the rib cage during inspiration elicits a marked increase in the inspiratory electromyographic (EMG) activity recorded from the external intercostal muscles but does not affect tidal volume (VT). In the present studies, we have tested the hypothesis that the maintenance of VT results from the concomitant contraction of the internal interosseous (expiratory) intercostals. When the rib cage was vibrated (40 Hz) during hyperventilation-induced apnea, a prominent activity was recorded from the external intercostals but no activity was recorded from the internal intercostals, including when the muscles were lengthened by passive inflation. The internal intercostals remained also silent when vibration was applied during spontaneous inspiration, and the phasic expiratory EMG activity recorded from them was unaltered when vibration was applied during expiration. Thus, the internal interosseous intercostals in dogs are much less sensitive to vibration than the external intercostals, and they do not interfere with the action of these latter during rib cage vibration. This lack of sensitivity might be the result of a reflex inhibition of the muscle spindle afferents by afferents from external intercostal muscle spindles.

Trajectory of single primary afferents from the intercostal muscle spindle in the cat

Although the corticospinal tract is not essential for the production of the basic locomotor rhythm in cats, it does contribute to the regulation of locomotion, particularly in situations in which there is a requirement for precise control over paw placement or limb trajectory. Lesions of the dorsolateral funiculi at the low thoracic level (T13) that completely interrupted both the cortico- and rubrospinal pathways produced long-term deficits in locomotion on a level surface. These deficits included a paw-drag that was probably caused both by a loss of cortico- and rubrospinal input to motoneurones controlling distal muscles as well as by a change in the relative timing of muscles acting around the hip and knee. Smaller lesions produced similar deficits from which the cats recovered relatively quickly. Cats with the largest lesions of the dorsolateral funiculi were unable to modify their gait sufficiently to step over obstacles attached to the treadmill belt even 3–5 months postlesion. These results imply that the medial pathways, the reticulo- and vestibulospinal pathways, are unable to fully compensate for damage to the lateral pathways. Single unit recordings from identified pyramidal tract neurones (PTNs) within the hindlimb representation of the primary motor cortex (area 4) showed that a substantial proportion of neurones (67%) significantly increased their discharge frequency when the cats modified their gait to step over obstacles attached to the treadmill belt. Of those PTNs that showed increased activity during the swing phase, populations of neurones were activated at different times. A large proportion of PTNS discharged early in swing, in phase with knee flexors such as the semitendinosus. Others discharged slightly later, in phase with the activity of ankle flexors, such as tibialis anterior, while still others discharged at the end of swing, in phase with digit dorsiflexors, such as the extensor digitorum brevis. We suggest that different populations of cortical neurones may specifically modify the activity of selected groups of close synergistic muscles during different parts of the swing phase. We further suggest that these modifications are mediated, in part, by groups of interneurones that are involved in determining the base locomotor rhythm. This provides a means by which the changes specified by the descending signal from the motor cortex may be smoothly, and appropriately, incorporated into the locomotor cycle.

1562 Trajectory of single primary afferents from the intercostal muscle spindle in the cat

Two thalamic sites are of especial significance for understanding hippocampal – diencephalic interactions: the anterior thalamic nuclei and nucleus reuniens. Both nuclei have dense, direct interconnections with the hippocampal formation, and both are directly connected with many of the same cortical and subcortical areas. These two thalamic sites also contain neurons responsive to spatial stimuli while lesions within these two same areas can disrupt spatial learning tasks that are hippocampal dependent. Despite these many similarities, closer analysis reveals important differences in the details of their connectivity and the behavioural impact of lesions in these two thalamic sites. These nuclei play qualitatively different roles that largely reflect the contrasting relative importance of their medial frontal cortex interactions (nucleus reuniens) compared with their retrosplenial, cingulate, and mammillary body interactions (anterior thalamic nuclei). While the anterior thalamic nuclei are critical for multiple aspects of hippocampal spatial encoding and performance, nucleus reuniens contributes, as required, to aid cognitive control and help select correct from competing memories.

Activity of the intercostal muscle spindle afferents in the lower thoracic segments during spontaneous breathing in the cat

Intraaxonal recordings of 33 spindle afferents from the inspiratory ( n = 8) and expiratory ( n = 25) intercostal muscles in the lower thoracic segments (T9-11), were made during spontaneous breathing in the anesthetized cat. All of them showed respiration-related activity. However, only three spindle afferents (one from the inspiratory and two from the expiratory intercostal muscles) showed higher firing frequency during the active contraction phase of the receptor-bearing muscle. The remaining 30 spindle afferents (seven from the inspiratory and 23 from the expiratory muscles) showed the maximum firing discharge during the passive stretch phase of the parent muscles. On the other hand, in the middle thoracic segments (T6-7), five of six spindle afferents from the inspiratory muscles and four of nine spindle afferents from the expiratory muscles showed maximum firing rate during parent muscle contraction in agreement with previous study. These results suggest that the spindle activity in the lower thoracic segments is dominated by muscle length changes, whereas that in the middle thoracic segments is largely via the fusimotor pathway.

Cerebral cortical evoked potentials elicited by cat intercostal muscle mechanoreceptors.

Intercostal muscle afferents discharge in response to changes in intercostal muscle mechanics and have spinal and brain stem projections. It was hypothesized that intercostal muscle mechanoreceptors also project to the sensorimotor cortex. In cats, the proximal muscle branch of an intercostal nerve was used for electrical stimulation. The mechanical stimulation was stretch of an isolated intercostal space. The sensorimotor cortex was mapped with a surface ball electrode. Primary cortical evoked potentials (CEP) were found in area 3a of the sensorimotor cortex with mechanical and electrical stimulation. The CEP was elicited with the smallest stretch amplitude used, 50 microns. The CEP response showed little increase beyond 300-microns stretch. The CEP elicited by 50-microns stretch suggests an initial cortical activation by intercostal muscle spindles. The minimal increase in CEP amplitude with stretch > 300 microns suggests that the CEP response is primarily due to muscle spindle recruitment. The increase in amplitude beyond this stretch may be due to recruitment of tendon organs. These results demonstrate a short-latency projection of intercostal muscle mechanoreceptors to the sensorimotor region of the cerebral cortex. This cortical activation may be involved in respiratory sensations and/or transcortical reflex responses to changes in respiratory muscle mechanics.

Medullary inspiratory activity: influence of intercostal tendon organs and muscle spindle endings.

Studies were conducted to determine the effects of intercostal muscle spindle endings (MSEs) and tendon organs (TOs) on medullary inspiratory activity in decerebrate and allobarbital-anesthetized cats. Impeded muscle contractions, elicited by electrical stimulation of the peripheral cut end of the T6 ventral root, were used to stimulate external and internal intercostal TOs without MSEs. Impeded contractions of either the external or internal intercostal muscles reduced phrenic and medullary inspiratory neuronal activities. Vibration was used to selectively stimulate external or internal intercostal MSEs (90 and 40 micron amplitude, respectively). Selective stimulation of either external or internal intercostal MSEs did not change phrenic or medullary inspiratory neuronal activities. It is concluded that both external and internal intercostal TOs have a generalized inhibitory effect on medullary inspiratory activity and intercostal MSEs have no effect on medullary inspiratory activity.

Medullary expiratory activity: influence of intercostal tendon organs and muscle spindle endings.

Studies were conducted to determine the effects of intercostal muscle spindle endings (MSEs) and tendon organs (TOs) on medullary expiratory activity in decerebrate cats. Impeded intercostal muscle contractions, elicited by electrical stimulation of the peripheral cut end of the T6 ventral root, were used to stimulate intercostal TOs without MSEs. Impeded contractions of the intercostal muscles augmented expiratory laryngeal motoneuron activity, and either had no effect on or reduced the activity of bulbospinal expiratory neurons. Vibration was used to stimulate intercostal MSEs. Intercostal MSEs had no effect on medullary expiratory neuron activity. It is concluded that both external and internal intercostal TOs have an excitatory effect on expiratory laryngeal motoneuron activity and an inhibitory effect on a subpopulation of expiratory neurons driving intercostal and/or abdominal muscles, and intercostal MSEs have no direct influence on medullary expiratory activity.

The effects of single afferent impulses on the probability of firing of external intercostal motoneurones in the cat.

1. Recordings of afferent discharges from external intercostal muscle spindles were made from in-continuity dorsal roots of anaesthetized, paralysed cats and the afferents were characterized as described in the preceding paper (Kirkwood & Sears, 1982).2. The strengths and time courses of the raised probabilities of firing of external intercostal motoneurones evoked by the synaptic actions of impulses in the afferents were measured by constructing cross-correlation histograms from the discharges of the individual afferents and the discharges of the motoneurones, which were simultaneously recorded from the cut central ends of intercostal nerve filaments. Other dorsal roots, apart from the rootlet containing the afferent fibre, were cut to prevent afferent synchronization from affecting the results.3. Cross-correlation histograms involving single efferent discharges showed narrow peaks (mean half-width 0.99 msec) at monosynaptic latencies.4. This mean half-width is slightly longer than the mean rise-time of the e.p.s.p.s described in the preceding paper, but much shorter than the mean half-width of those e.p.s.p.s. These measurements, together with the shapes of individual histogram peaks thus confirm the prediction of Kirkwood & Sears (1978) that the shape of such a peak should be approximated by the time differential of the underlying e.p.s.p. plus the e.p.s.p. time course itself. Amplitudes of the peaks were also consistent with the predictions of Kirkwood & Sears (1978).5. The cross-correlation histograms involving multi-unit efferent discharges were entirely consistent with those involving single efferent discharges and were used to demonstrate the patterns of projections of individual afferents to different groups of intercostal motoneurones.6. Individual afferents excited alpha motoneurones of all spike sizes in the intercostal filament recordings but excitation of gamma motoneurones was not detected.7. Individual afferents excited motoneurones of the same segment and both adjacent segments, but no projection beyond these was detected.8. The amplitude of the multi-unit cross-correlation peak was taken as a measure of the over-all strength of the connexions to a given segment. When this amplitude was measured for motoneurones of the same segment as the afferent, for sixteen out of nineteen afferents there was a highly significant positive correlation with the conduction velocity of the afferent. The remaining three afferents gave a strength of connexion which appeared to be much stronger than would be expected from the rest of the population of afferents.9. The strength of connexion to adjacent segments was generally lower than to the same segment.

Thoracic dorsal rhizotomy in the anesthetized cat: Maintenance of eupnic breathing

In order to assess the level of participation of thoracic afferents in the determination of the eupnic breathing pattern, thoracic dorsal rhizotomies from T1 through T13 were performed in cats anesthetized with α-chloralose or sodium pentobarbital, with or without intact vagi. While recording several respiratory parameters, no consistent changes in the spontaneous breathing pattern could be demonstrated either 10–20 min or 90–100 min following disruption of thoracic afferent input. Thus, respiratory frequency, tidal volume and total ventilation were unaffected by rhizotomy. Inspiratory (T i) and expiratory (T e) durations and T i/T e ratios remained constant. Tracheal air flows during inspiration and expiration and intrapleural pressure were not altered. Finally, end-expiratory %CO 2 and %O 2 did not change after section of the thoracic dorsal roots. Only arterial blood pressure was found to fall as a function of time into the experiment. Since the results were identical in vagotomized and in vagi intact preparations, thoracic reflexes were not being masked by vagal dominance in eupnea. Rather, thoracic afferents, including intercostal muscle spindle afferents, appear to be ineffective in shaping the pattern of quiet breathing in anesthetized cats. This is unlike situations of loaded or stressed breathing where these afferents assume a more active role in the modulation of rate and depth mechanisms.

Neonatal chest wall afferents and regulation of respiration

We have studied two groups of eight preterm infants, relating chest wall afferent information to respiratory timing. Rib cage and abdominal motion were monitored by magnetometers and flow and tidal volume via a face mask. In the first group, studies were done in REM sleep when spontaneously occurring distortion of the rib cage occurred and a significant linear relationship between the rate of distortion of the chest wall and shortening of the inspiratory time (Ti) was found in all infants. Reduction in this distortion by the use of continuous positive airway pressure (CPAP) or continuous negative pressure at the body surface (CNeg) was associated with a significant (P less than 0.01) lengthening of Ti. Absence of changes in Ti when pressure was applied in quiet sleep suggested that lung volume or chemical changes were not involved. In the second group of infants we artificially generated the afferent inflow by using vibratory stimuli applied in one intercostal interspace and produced a significant (P less than 0.05) shortening in Ti. We suggest that the distortion of the rib cage in REM sleep generates afferent information from intercostal muscle spindles that is related to the rate of distortion and this, via a supraspinal reflex, inhibits phrenic motoneuron discharge. It may then be of importance in the etiology of apneic episodes in these infants. Applied pressure may be of benefit because it reduces an inhibitory afferent inflow.

Changes in the pattern of breathing caused by chest vibration

Vibration of 100 Hz was delivered longitudinally onto the sternum of anaesthetized cats and rabbits. Vibration consistently reduced the tidal volume by 10–15% without altering the end-expiratory point, and occasionally reduced the respiratory rate. Vibration applied during inspiration reduced the tidal volume as much as if delivered over several breaths. Expiratory vibration did not alter the course of the expiration, nor the volume of the following inspiration. The inhibition of inspiration was unaffected by deaffcrcntation of chest wall skin, bilateral vagotomy, bilateral division of the phrenic nerves and low thoradc spinal transection. Spinal tranaection above the thoracic cord (C8/T1) abolished usual responses to vibration. The receptors for this reflex probably lie in the chest wan. Vibration inhibited the development of alae nasi tension during inspiration indicating that supraspinal reflex loops were involved. A role for intercostal muscle spindles is suggested.

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.

The response of the respiratory system to elastic loading in cats

The respiratory response to the imposition and maintenance of an elastic load was studied in cats. The first loaded breath showed the following changes from control : an increase in inspiratory duration, a rise in the change of oesophageal pressure with inspiration (ΔP i-e), a fall in tidal volume, and an increase in the total integrated e.m.g. of both diaphragmatic and inspiratory intercostal muscles. Activity mediated by the vagus nerves was responsible for 62% of the response, and this was solely due to prolongation of inspiration. This inspiratory prolongation was abolished by cooling the vagus nerves to 6–8°C and could, therefore, result from the fall in stretch afferent discharge that occurs. The remaining response was probably due to the mechanical properties of the inspiratory muscles since there was little evidence to suggest that feedback from intercostal muscle spindles produced a positive response. The response increased progressively as the load was maintained and this could be due to the rapid changes in carotid artery Pa CO 2 which were found.

Inhibition of inspiratory activity by intercostal muscle afferents

Thoracic mechanoreceptors inhibit phrenic and inspiratory intercostal discharge in anesthetized, vagotomized cats and dogs. Each of three mechanical stimuli, chest compression, intercostal muscle stretch and rib vibration, inhibits phrenic discharge and each provides evidence that intercostal muscle spindles contribute to this reflex. Phrenic inhibition by airway occlusion is probably accounted for by this reflex. Alterations of respiratory rhythm indicate that supra-spinal reflexes are initiated by the mechanical stimuli. An inspiratory inhibition reflex from intercostal muscle spindles might act to increase the mechanical efficiency of breathing.

The proprioceptive reflex control of the intercostal muscles during their voluntary activation.

1. A quantitative study has been made of the reflex effects of sudden changes in mechanical load on contracting human intercostal muscles during willed breathing movements involving the chest wall. Averaging techniques were applied to recordings of electromyogram (EMG) and lung volume, and to other parameters of breathing.2. Load changes were effected for brief periods (10-150 msec) at any predetermined lung volume by sudden connexion of the airway to a pressure source variable between +/- 80 cm H(2)O so that respiratory movement could be either assisted or opposed. In some experiments airway resistance was suddenly reduced by porting from a high to a low resistance external airway.3. Contracting inspiratory and expiratory intercostal muscles showed a ;silent period' with unloading which is attributed to the sudden withdrawal from intercostal motoneurones of monosynaptic excitation of muscle spindle origin.4. For both inspiratory and expiratory intercostal muscles the typical immediate effect of an increase in load was an inhibitory response (IR) with a latency of about 22 msec followed by an excitatory response (ER) with a latency of 50-60 msec.5. It was established using brief duration stimuli (< 40 msec) that the IR depended on mechanical events associated with the onset of stimulation, whereas stimuli greater than 40 msec in duration were required to evoke the ER.6. For constant expiratory flow rate and a constant load, the ER of expiratory intercostal muscles increased as lung volume decreased within the limits set by maximal activation of the motoneurone pool as residual volume was approached.7. The ER to a constant load increased directly with the expiratory flow rate at which the load applied, also within limits set by maximal activation of the motoneurone pool.8. For a given load, the ER during phonation was greater than that occurring at a similar expiratory flow rate without phonation when the resistance of the phonating larynx was mimicked by an external airway resistance.9. It is argued that the IR is due to autogenetic inhibition arising from tendon organs and that the ER is due to autogenetic excitation arising from intercostal muscle spindles.10. The initial dominance of inhibition in this dual proprioceptive reflex control was not predicted by the servo theory. It is proposed that the reflex pathways subserving autogenetic inhibition are under a centrifugal control which determines in relation to previous experience (learning) the conditions under which autogenetic facilitation is allowed.

Fusimotor effects on position and velocity sensitivity of spindle endings in the external intercostal muscles of the cat.

AbstractPosition and velocity responses of spindle endings in the external intercostal muscle of the cat have been determined in the absence and in the presence of fusimotor fibre stimulation at a constant rate. The length input signal had triangular wave form. A close functional resemblance was found between intercostal and leg muscle spindles: primary and secondary endings could be separated among intercostal afferents with the same methods that have been used in leg muscles; dynamic and static fibres were discerned and the fusimotor effects on position and velocity sensitivity were the same as in the hind limb; the ratio between dynamic and static fibres was about 1: 3, i.e. the same as in the hind leg. Some dissimilarities existed: the number of ‘intermediate’ endings was larger in the intercostal than in the leg muscles; position and velocity sensitivities were generally larger in intercostal endings. These discrepancies are discussed. As a general conclusion it is stated that a spindle model elaborated from studies on leg spindles can easily be modified to account also for intercostal spindle behaviour.

Fusimotor Effects on Position and Velocity Sensitivity of Spindle Endings in the External Intercostal Muscle of the Gat

AbstractPosition and velocity responses of spindle endings in the external intercostal muscle of the cat have been determined in the absence and in the presence of fusimotor fibre stimulation at a constant rate. The length input signal had triangular wave form. A close functional resemblance was found between intercostal and leg muscle spindles: primary and secondary endings could be separated among intercostal afferents with the same methods that have been used in leg muscles; dynamic and static fibres were discerned and the fusimotor effects on position and velocity sensitivity were the same as in the hind limb; the ratio between dynamic and static fibres was about 1: 3, i.e. the same as in the hind leg. Some dissimilarities existed: the number of ‘intermediate’ endings was larger in the intercostal than in the leg muscles; position and velocity sensitivities were generally larger in intercostal endings. These discrepancies are discussed. As a general conclusion it is stated that a spindle model elaborated from studies on leg spindles can easily be modified to account also for intercostal spindle behaviour.