Muscle afferent function and its significance for motor control mechanisms during voluntary movements in cat, monkey, and man.
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Biomedical subjects
Publications and source records attributed to M Hulliger.
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The impulse discharge in single afferent units from muscle spindles was recorded in waking human subjects, using tungsten needle electrodes which were percutaneously inserted in the radial nerve. Eighteen spindle afferents from the finger extensor muscles were studied, 11 primaries and 7 secondaries. The subjects performed standardized trapezoidal finger movements in a visual tracking task which included periods of position holding. A load of constant torque opposed finger extension. Its size was varied with successive tests and covered up to 29% of the maximum voluntary contraction force (MVF). The mean discharge of the afferent unit during holding was measured and related to the size of the load. The mean discharge rate of both primary and secondary units increased with the size of the load. There was considerable scatter of the data points, but generally a linear relationship was an acceptable describing function. For the pooled data of the total sample of primaries the slope was 0.47 impulses/s/%MVF, whereas the corresponding figure for the secondaries was 0.66 impulses/s/%MVF after an appropriate correction for a sampling bias. The rates of discharge of the present sample of units were generally low in relation to those reported for afferents from, for instance, ankle muscles in the cat. The rise of spindle discharge with increasing size of the load indicated that a broad parallelism of skeleto- and fusimotor activity was present during accurate position holding. However, there were indications that a rigid linkage between total skeletomotor activity and the fusimotor drive to individual spindles was not present.
Surface EMG activity from the first dorsal interosseus, time-locked to twitch contractions in the same muscle, was investigated using the technique of spike-triggered averaging. A decrease in surface EMG activity was observed during the rising phase of twitch force, consistently followed by two bursts of activity with roughly constant onset latencies. One burst occurred at 45 msec from the onset of the single motor unit potential used to trigger the averager and was near the peak of the twitch contraction. The other burst occurred at 77 msec during the falling phase of the twitch contraction. If it is assumed that the chance synchronization of motor units contributes to physiological tremor [1, 5, 20], then the observed relative strengths of the two bursts of EMG activity indicate that their net action could enhance tremor.
After-effects of fusimotor action on dynamic sensitivity of spindle primary afferents from soleus resulted from low rate stimulation of both static and dynamic gamma-axons. Sensitivity to small sinusoidal stretches superimposed on triangles was enhanced during triangular lengthening but not during shortening. These after-effects were elicited by fusimotor stimulation during preceding triangular shortening, but not during lengthening. Given these characteristics, they may be important functionally during alternating rhythmic movements.
The actions elicited by electrical stimulation of the rubrospinal path in NR (nucleus ruber), and by stimulation of the rubro-bulbospinal path in MesADC (mesencephalic area for dynamic control), were studied with intra-, juxta- or extracellular recordings in lumbar gamma-motoneurones of cats anaesthetized with chloralose. The results were obtained during a series of experiments in which reflex effects from muscle, skin and joint afferents were also investigated. 90 cells tested with stimulation both in NR and in MesADC were classified (cf. Appelberg 1981) as dynamic (influenced from MesADC) or static (not influenced). 84 of these gamma-cells responded to stimulation in the red nucleus. The same response pattern was found for dynamic and static gamma-cells. For flexor cells, excitation was by far predominant while equal numbers of extensor cells showed excitatory and inhibitory effects. The shortest route to both static and dynamic gamma-cells was disynaptic. With stimulation of the rubro-bulbospinal path, excitatory effects were more than twice as frequent as inhibitory effects. No clearcut difference was seen between extensor and flexor cells. The segmental latency for rubro-bulbospinally mediated excitatory effects could be measured for only one cell, and it is tentatively suggested that the pathway to this dynamic gamma-motoneurone involves one or two interneurones more than in the rubrospinal pathway. Spontaneous activity was significantly more common among the dynamic cells, but the axonal conduction velocities of dynamic and static cells did not differ. The similarities between rubro-spinal effects on alpha-motoneurones and both classes of gamma-motoneurones indicate that the rubrospinal tract has the ability to coactivate alpha- and gamma-motoneurones (Granit 1955, 1979). The comparison of the properties of the population of gamma-cells classified as dynamic or static showed marked differences strengthening the reliability of the previously introduced classification method.
1. Single unit activity of muscle spindle afferents from finger extensor muscles was recorded in the radial nerve of waking human subjects. The mean discharge rate of the afferent units was determined while the receptor related finger was held at fixed angular positions of the metacarpo-phalangeal joint. 2. During a visual tracking task the subjects had to maintain specified angular positions against a load of constant torque which opposed finger extension. For each unit a comparison was made between the mean discharge rates at two angular positions which differed by 20 deg. Under such isotonic conditions the rates of afferent discharge at the two joint positions did not significantly differ, neither for the whole sample of primary, nor for that of secondary units. This was true, no matter whether the load was small or intermediate. Large loads were not tested. 3. For comparison, the passive position responses of a sample of spindle afferent units from the same muscles were studied when the finger was held in fixed positions while the muscles were voluntarily relaxed. Under these conditions a significant position sensitivity was found for both primary and secondary afferents. The mean values were 0.28 impulses/sec. deg (primaries), and 0.21 impulses/sec. deg (secondaries). 4. The absence of position response during active position holding was interpreted as a manifestation of changes in fusimotor outflow which depended on joint position and were large enough to compensate for changes in muscle length.
1. Experiments were performed in forty-one cats anaesthetized with chloralose.2. The aim of the study was to investigate whether activity in stretch-sensitive muscle receptors may cause reflex effects in fusimotor neurones.3. Activity in fusimotor neurones was studied indirectly by recording from primary and secondary muscle spindle afferents of the triceps surae muscle. The mean rate of firing of the afferents as well as either dynamic index (during ramp extension) or modulation (during sinusoidal extension) was determined. This was done under control conditions, with the posterior biceps-semitendinosus muscles relaxed, and under test conditions, with the same muscles extended.4. All together, seventy-one primary afferents were studied quantitatively. Pure or predominantly dynamic effects were observed in twenty-two, pure or predominantly static effects in nine and no statistically significant effects in forty of the units. Amongst seven secondary afferents studied, two showed weak fusimotor activation, the other five were not influenced.5. Electrical stimulation of the posterior biceps-semitendinosus or medial gastrocnemius nerves at group II strength was observed to cause dynamic fusimotor reflexes on a number of occasions.6. The reflex effects observed were, on many occasions, recorded in spinalized preparations.7. The reflex effects were not accompanied by any detectable e.m.g. activity in triceps, as judged from surface e.m.g. recordings. The reflex effects observed are therefore tentatively ascribed to activation of gamma-motoneurones, yet a contribution from beta-motoneurones cannot wholly be excluded.8. On the basis of available evidence concerning reflex connexions to gamma-motoneurones from various muscle afferents, it is suggested that the effects observed were caused by activation of muscle spindle secondary endings.
The activity of human muscle spindle afferents from finger extensor muscles has been studied during voluntary movements in a visual tracking paradigm. With an elastic load the spindle discharge rate was disproportionately high when the opposing force was close to zero, suggesting that the fusimotor drive was high when the direct afferent information about the size of the load that the subject had to handle was poor.
The activity of human spindle afferents from finger extensor muscles has been studied during voluntary position holding at two finger positions, to disclose any explicit monitoring of muscle length. The results indicate that, taken as groups, neither primary nor secondary afferents show explicit position responses during active position tracking. Thus any contribution from muscle spindle to position sense must be derived from other components in spindle afferent discharge.
The interaction of static and dynamic fusimotor activation on the firing of primary muscle spindle afferents has been studied in the cat soleus muscle at constant length and during sinusoidal stretching. Cycle histogram analysis revealed summation of static and dynamic action during the peak of the afferent response to sinusoidal stretching, while static action completely occluded the dynamic effect during the trough of the response. Occlusion was complete as long as, for single fusimotor activation, the static-induced trough response exceeded the dynamic-induced one by about 25%. The investigation of inter-spike interval distributions obtained at constant muscle length revealed occlusion of dynamic by static action in 8 out of 13 cases. A model of multiple spike generation in primary spindle afferents is considered which is based on two or more pacemakers arranged in parallel, with a common pacemaker in series.
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Experiments in mice were performed in order to investigate whether vagal activity could affect glycoprotein secretion from gallbladder principal cells. This cell type was studied with the electron microscope in control animals and after electric stimulation of the right or left nervus vagus. The volume density of glycoprotein containing granules was determined using morphometry. It was found that stimulation of the left vagus nerve significantly reduced the relative cellular volume of secretory granules in the principal cells of the gallbladder. Right vagus stimulation was accompanied by a weak but insignificant increase in secretory granule content. It is suggested that the left vagus nerve may exert a direct influence on glycoprotein secretion from gallbladder principal cells.
1. Afferent activity of 111 single units from the glabrous skin area was recorded percutaneously in the median nerve of human subjects, using tungsten electrodes. 2. The majority of the units (103) were classified as low-threshold mechano-sensitive units belonging to one of the four categories previously described: rapidly adapting with small receptive fields (RA), rapidly adapting with large receptive fields (PC, presumed Pacinian corpuscle units), slowly adapting with small fields (SA I), and slowly adapting with large fields (SA II). The size of the responses (in number of impulses) to indentation and stretching of the skin was compared with that of the responses elicited during voluntary isotonic finger movements, which avoided trivial excitation of the units by direct touch. 3. All four types of units, and 77% of the single units, were activated by isotonic movements. The decreasing order of responsiveness was PC, SA II, SA I, RA. 4. Almost all responsive units were excited during the dynamic phase of ramp and smooth oscillatory movements. Static responses, on the other hand, occurred only with 50% of the slowly adapting units, corresponding to a third of the total sample (SA II, 81%; SA I, 17%. 5. For all four types of units the dynamic responses to movements were of similar size as the responses to localized skin indentation with a von Frey hair at five times threshold. 6. The results are discussed with regard to the possible implications for kinaesthesia and motor control.
1. Single fusimotor fibres to de-efferented soleus of the cat were stimulated to investigate the size and time course of the responses elicited in single primary spindle afferents. The muscle was kept at constant length close to the physiological maximum. Constant and alternating rates of fusimotor stimulation were used: (a) repetitive stimulation at constant rate (maintained stimulation); (b) modulated stimulation with the rate of activation alternating between two constant levels at repeat frequencies between 0.09 and 2 Hz (rectangular stimulation). The responses were averaged and displayed as post-stimulus time (pst) histograms (a) or as cycle histograms (b). 2. During static fusimotor stimulation the pst histograms could be clearly modulated over a range of rates of stimulation. However, histogram modulation was not a prerequisite of static action since with different fibres the degree of modulation could range from deeply modulated to completely non-modulated to completely non-modulated. 3. Dynamic fusimotor stimulation was almost always accompanied by non-modulated pst histograms. 4. Primary spindle afferents responded to rectangular stimulation of either kind of fusimotor fibre with an approximately rectangular modulation of the rate of discharge. At the repeat frequencies studied the size of the responses was appreciably larger with static than with dynamic activation. It was assessed as 'fusimotor rate-sensitivity during alternating stimulation' by the response/stimulus ratio which is defined as change in firing/change in alternating rate of stimulation, in impulses/stimuli. The mean values of rate-sensitivity were 1.35 impulses/stimuli (statics) and 0.29 (dynamics), with a static/dynamic ratio of 4.7. 5. The afferents' 'fusimotor rate-sensitivity during steady stimulation' (change in firing/change in maintained rate of stimulation( was also determined. The mean values were 0.78 (static) and 0.37 (dynamics), with a static/dynamic ratio of 2.1. 6. The time course of the responses to rectangular stimulation was of the same order of magnitude for static and dynamic fibres. It was assessed by fitting a single exponential to the rising and falling phase of cycle histograms. The mean values of the time constants for static fibres were 58 msec (rising phase) and 59 msec (falling phase), and for dynamic fibres 34 msec (rising phase) and 49 msec (falling phase). The differences were statistically non-significant. 7. The significance of the modulation in pst histograms and the mechanisms and functional implications of the differences in rate-sensitivity are discussed. It is concluded that at constant muscle length static and dynamic fusimotor fibres differ significantly by the size rather than the speed of their action on primary spindle afferents.
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