Mikael Bergenheim

Alterations in information transmission in ensembles of primary muscle spindle afferents after muscle fatigue in heteronymous muscle.

This study showed that fatigue of the ipsilateral medial gastrocnemius muscle caused a clear-cut reduction in the ability of ensembles of primary muscle spindle afferents from the lateral gastrocnemius muscle to discriminate between muscle stretches of varying amplitude. The results were probably caused by reflex-mediated effects from chemosensitive group III and IV afferents onto the gamma-motoneurons projecting to lateral gastrocnemius muscle spindles. The experiments were conducted on seven cats anaesthetized with alpha-chloralose and a total of 41 primary muscle spindle afferents from the lateral gastrocnemius were registered. Afferents were simultaneously recorded in ensembles of three to 10 afferents. A method based on principal component analysis and algorithms for quantification of stimulus discrimination in ensembles of muscle afferents was used prior to, immediately following and five or more minutes after muscle fatigue had been induced to the ipsilateral medial gastrocnemius muscle. It is well established that the primary muscle spindle afferents play an important role in proprioception and kinaesthesia. Therefore the decrease in the accuracy of the information transmitted by ensembles of primary muscle spindle afferents caused by fatigue in an ipsilateral muscle implies concomitant effects on proprioception and kinaesthesia.

Influences on the γ-muscle spindle system from muscle afferents stimulated by increased intramuscular concentrations of bradykinin and 5-HT

There is evidence that static muscular contractions induce a release of bradykinin (BK) in the working muscle, and that increased concentration of BK and 5-HT in a muscle increases the discharge rate of a subpopulation of group III and group IV muscular afferents. It is also known that activity in group III and IV muscle afferents may activate gamma-motoneurones to both homonymous and heteronymous muscles. The aim of the present study was to investigate whether increased concentration of BK and 5-HT in one muscle may influence the activity in primary and secondary muscle spindle afferents (MSAs) from the chemically affected muscle and from surrounding muscles, via fusimotor reflexes. The experiments were made on six cats anaesthetised with alpha-chloralose. The triceps surae (GS) and the posterior biceps and semitendinosus (PBSt) muscles were subjected to sinusoidal stretches. Simultaneous recordings of 2-11 MSAs from these muscles were made and the mean rate of firing and the modulation for each MSA were determined. Responses of 47 MSAs (26 PBSt and 21 GS) were recorded. The responsiveness of the MSAs to injections of BK (9-100 mg/ml, 0.5-1.0 ml) and 5-HT (25-150 mg/ml, 0.5-1.0 ml) was 89% and 83%, respectively, for injections into the arterial supply of the ipsilateral GS muscle, and 84% and 40% respectively for injections to the contralateral GS muscle. Of 10 secondarŁy MSAs, only one was unresponsive to BK injections, while several MSAs responded to both ipsilateral and contralateral BK injections.(ABSTRACT TRUNCATED AT 250 WORDS)

Influences on the fusimotor-muscle spindle system from chemosensitive nerve endings in cervical facet joints in the cat: possible implications for whiplash induced disorders

&NA; The aim of the present study was to establish if there exists reflex connections from ligamentous structures in cervical facet joints and the fusimotor system of dorsal neck muscles. In seven cats, anaesthetized with &agr;‐chloralose, bradykinin (BK) of concentrations between 12 and 50 &mgr;g was injected into the facet joint between C1 and C2. Recordings were made from single muscle spindle afferents (MSA) originating in contralateral trapezius and splenius muscles (TrSp). Fusimotor induced changes in the sensitivity of the muscle spindle afferents were assessed by recording the responses to sinusoidal stretches of the TrSp muscles. The mean rate of discharge and the depth of modulation of a fitted sine were taken as quantitative estimates of the response. A total of 25 MSAs were recorded, and 21 of these showed clear‐cut alterations in their responses to the sinusoidal stretches following Bk. injections into contralateral facet joint. The majority of the responding afferents (13/21) showed changes in their responses indicating an increased activity of static fusimotoneurones, although responses of dynamic and mixed static and dynamic nature were also seen. Local anaesthetics applied to the intraarticular receptors abolished the effects. Injection (i.v.) of a general anaesthetic (pentobarbital) abolished the effects. The results show that there exist reflex connections between receptors in cervical facet joints and fusimotoneurones of dorsal neck muscles, and this might be of importance in the pathophysiology behind whiplash associated disorders (WAD).

Influences on the γ-muscle-spindle system from muscle afferents stimulated by increased intramuscular concentrations of arachidonic acid

There is evidence that static muscular contractions induce a release of arachidonic acid (AA) in the working muscle and that increased concentration of AA in a muscle increases the discharge rate of a subpopulation of groups III and IV muscular afferents. It is also known that activity in groups III and IV muscle afferents may activate gamma-motoneurones to both homo- and heteronymous muscles. The aim of the present study was to investigate if increased concentration of AA in one muscle may influence the activity in primary and secondary muscle spindle afferents (MSAs) from the chemically affected muscle and from surrounding muscles, via fusimotor reflexes. The experiments were made on five cats anaesthetized with alpha-chloralose. The triceps surae (GS) and the posterior biceps and semitendinosus (PBSt) muscles were subjected to sinusoidal stretches. Simultaneous recordings of 2-12 MSAs from these muscles were made and the mean rate of firing and the modulation for each MSA were determined. Responses of 36 MSAs (17 PBSt and 19 GS) were recorded. The responsiveness of the MSAs to injections of AA (0.3-1.0 mg; 0.3-1 ml) was 86% (n = 36) for injections into the arterial supply of the ipsilateral GS muscle and 45% (n = 20) for injections to the contralateral GS muscle. Out of 14 secondary MSAs, only one was unresponsive to ipsilateral AA injections while two of eight were unresponsive to contralateral AA injection. The majority of responses were compatible with predominantly static or mixed dynamic and static fusimotor activation. None of the effects were compatible with inhibition of fusimotor activity. The duration of the effects were usually 2-4 min. However, on some occasions the elevations in MSA activity persisted for up to 1 h. Local anaesthesia of the nerve to the injected muscle always abolished the effects of the injections and control injections of the solution in which the AA was dissolved were ineffective in changing the MSA responses. I.v. injections occasionally induced effects on the MSAs, but such effects were significantly different from those caused by close arterial muscle injections. Thus, increased concentration of AA may excite primary and secondary MSAs from homo- as well as heteronymous muscles, including contralateral muscles, most probably via fusimotor reflexes evoked by activity in chemosensitive muscle afferents.

Elevated Intramuscular Concentration of Bradykinin in Jaw Muscle Increases the Fusimotor Drive to Neck Muscles in the Cat

Patients suffering from temporomandibular dysfunction exhibit clinical findings such as fatigue, painful muscles, and muscles that are tender to palpation, not only in the temporomandibular area, but also in the neck/shoulder region. The mechanisms behind this are not known, although previous studies of similar spreading phenomena have revealed a possible involvement of the fusimotor system. In the present study, we evaluated the activity of this system by recording the activity of muscle spindle afferents from dorsal neck muscles after intramuscular injections of 6 μg to 25 μg bradykinin in the ipsilateral masseter muscle. A total of 23 muscle spindle afferents from the trapezius and splenius muscles was recorded at the C3-C4 level in 7 adult cats anesthetized with a-chloralose. Of these 23 afferents, 17 (74%) showed significantly different responses to bradykinin injections compared with control injections (dissolving agent, Tyrode), and the majority of the effects were compatible with an increased static fusimotor drive to the muscle spindle system. Thus, the results demonstrate potent reflex connections from groups III and IV masseter muscle afferents to fusimotor neurones on the C3-C4 level. It is concluded that the fusimotor system might play a significant role in the mechanisms behind the spread of muscle pain and tension from the temporomandibular region to the neck.

Influences on the γ-muscle-spindle system from contralateral muscle afferents stimulated by KCl and lactic acid

The aim of the present study was to investigate whether increased concentrations of lactic acid and potassium chloride (KCl) in contralateral muscles can influence the sensitivity of primary and secondary muscle spindle afferents (MSAs) from ipsilateral extensor and flexor muscles. The experiments were performed on 7 cats anaesthetised with alpha-chloralose. Recordings were made simultaneously from 2-12 single MSAs from the triceps surae (GS) and/or the posterior biceps and semitendinosus muscles (PBSt). The mean rate of firing and the amplitude of a fitted sine curve of MSA responses to sinusoidal stretching of the receptor bearing muscles were determined. Responses of 42 primary MSAs (17 from PBSt and 25 from GS) were recorded. On 33 of these, clear-cut alterations in sinusoidal response were evoked by injection of 1 ml KCl (200-400 mM) or 1 ml lactic acid (20-50 mM) into the arterial supply of the contralateral GS or PBSt muscles. Six out of 8 secondary MSAs showed sizeable effects to increased intramuscular concentrations of KCl and/or lactic acid (3 from PBSt and 3 from GS). On both primary and secondary MSAs, from GS as well as from PBSt muscles, the large majority of effects were excitatory. All effects on secondary MSAs were compatible with reflex actions on static fusimotor neurones, whereas on primary MSAs different types of reflex responses were observed (i.e. pure static, pure dynamic and mixtures of static and dynamic fusimotor actions). Stimuli related alterations in MSA responses were completely abolished when the contralateral GS or PBSt nerves were anaesthetised.(ABSTRACT TRUNCATED AT 250 WORDS)

BRADYKININ AND MUSCLE STRETCH ALTER CONTRALATERAL CAT NECK MUSCLE SPINDLE OUTPUT

The objective of this study was to investigate the activity of primary and secondary muscle spindle afferents (MSAs) in neck muscles, when the contralateral splenius or trapezius muscles were (1) exposed to i.m. injection of bradykinin (BK) (6-86 microg/ml), (2) stretched, (3) stretched during exposure to BK or (4) stretched after exposure to BK. It was found that injection of BK, muscle stretch and the combination of the two stimuli significantly excited primary and secondary MSAs via reflex effects onto static fusimotor neurones. BK, alone, and in combination with muscle stretch, induced more frequent, potent and long lasting effects as compared to muscle stretch. The effects of muscle stretch was significantly increased after exposure of BK, indicating that stretch-sensitive nerve-endings within neck muscles are sensitised by BK. The results are discussed in relation to the disturbances in motor co-ordination and proprioception found in patients suffering from chronic muscle pain in the cervical region.

The role of the γ-system for improving information transmission in populations of Ia afferents

Abstract Ensemble coding of simple mechanical stimuli (small sinusoidal stretches) was studied in populations of simultaneously recorded primary muscle spindle afferents (MSAs). The experiments were made on 39 primary MSAs in choralose anaesthetised cats. For the analyses we used a combination of principal component analysis and algorithms for quantification of stimulus discrimination. Ensembles of primary MSAs discriminated better between different muscle stretches than individuals, and showed a successive increase in discriminative ability with increasing ensemble size. The ensemble effect disappeared after cutting the ventral roots, indicating an important role for the fusimotor system in ensemble coding. Simultaneously recorded ensembles of MSAs showed significantly better discriminative ability than pooled sequentially recorded MSAs. This difference was abolished by the cutting of the ventral roots. It is hypothesised that, since the muscle spindles are connected to each other via secondary MSAs (projecting to γ-motoneurones to other spindles), the fusimotor-muscle spindle system may constitute a neural network, in which each ‘neuron’ (i.e., each individual muscle spindle) is influenced by the activity in the whole network. In populations of pooled sequentially recorded MSAs, the connections would not exist. Thus, the population would lose its neural network quality, and the encoding ability of the population would decrease.

Inducing Any Virtual Two-Dimensional Movement in Humans by Applying Muscle Tendon Vibration

In humans, tendon vibration evokes illusory sensation of movement. We developed a model mimicking the muscle afferent patterns corresponding to any two-dimensional movement and checked its validity by inducing writing illusory movements through specific sets of muscle vibrators. Three kinds of illusory movements were compared. The first was induced by vibration patterns copying the responses of muscle spindle afferents previously recorded by microneurography during imposed ankle movements. The two others were generated by the model. Sixteen different vibratory patterns were applied to 20 motionless volunteers in the absence of vision. After each vibration sequence, the participants were asked to name the corresponding graphic symbol and then to reproduce the illusory movement perceived. Results showed that the afferent patterns generated by the model were very similar to those recorded microneurographically during actual ankle movements (r=0.82). The model was also very efficient for generating afferent response patterns at the wrist level, if the preferred sensory directions of the wrist muscle groups were first specified. Using recorded and modeled proprioceptive patterns to pilot sets of vibrators placed at the ankle or wrist levels evoked similar illusory movements, which were correctly identified by the participants in three quarters of the trials. Our proprioceptive model, based on neurosensory data recorded in behaving humans, should then be a useful tool in fields of research such as sensorimotor learning, rehabilitation, and virtual reality.

Increased intra-articular concentration of bradykinin in the temporomandibular joint changes the sensitivity of muscle spindles in dorsal neck muscles in the cat.

The aim of the present study was to investigate to what extent activation of bradykinin-sensitive nerve endings of the temporomandibular joint (TMJ) might induce changes in the muscle spindles output from neck muscles through reflex effects on cervical fusimotor neurones. To this end, 26 muscle spindle afferents (MSAs) emanating from the trapezius and splenius muscles of the anaesthetised cat (alpha-chloralose, initial dosage 60 mg/kg) were recorded during injection of Bradykinin (BK) (12.5-50 microg/ml) in the ipsilateral TMJ. Fifteen (58%) MSAs exhibited statistically significant fusimotor effects to injection of BK into the TMJ. Of the 15, ten MSAs showed a response related to activation of static fusimotor neurones, three MSAs showed a response related to an activation of both static and dynamic fusimotor neurones and two MSAs showed a inhibition of both static and dynamic fusimotor neurones. The control experiments suggests that the effects observed were due to activation of BK sensitive nerve endings in the TMJ. It seems possible that the reflex connections between TMJ nociceptors and the fusimotor-muscle spindle system of dorsal neck muscles might be involved in the pathophysiological mechanisms responsible for the sensory-motor disturbances in the neck region often found on patients with temporomandibular disorders.