Dual response from human muscle spindles in fast voluntary movements.

Single-unit impulses were recorded from the radial nerve of attending human subjects using the microneurography technique. The discharge of muscle spindle afferents from the extensor digitorum muscles was analysed while subjects performed fast lengthening and shortening voluntary movements as well as movements of moderate speed at a single metacarpophalangeal joint. Opposing or assisting loads of moderate size were added in some tests. Fast lengthening movements were, in practically all units, associated with acceleration of spindle discharge. However, the responses were modest and in many primary afferents it was of similar size as their response to small irregularities during slower movements. During shortening movements, most spindle afferents stopped firing altogether, whereas some afferents exhibited a distinct burst of impulses at the onset of active shortening followed by silence during the main part of the movement. This initial shortening responses was sometimes more prominent when the parent muscle worked against an opposing load. It was interpreted as a result of fusimotor drive associated with the building up of force in the contracting muscle. The initial shortening response from the contracting muscle and the stretch response from the antagonist constitute a dual signal, describing accurately the onset of joint movement as seen from the two muscles. It remains to be clarified which role this pattern of afferent responses may have in the design of the current motor output and in the capturing of nature and size of the external load.

Lack of fusimotor modulation in a motor adaptation task in man.

Single-unit activity was recorded from the radial nerve of human subjects along with surface electromyogram, joint angle, velocity, and torque at a metacarpophalangeal joint. Nine afferents from muscle spindles in the extensor digitorum muscles were studied in a motor adaptation task which involved modulations of the long-latency stretch reflex. While subjects slowly moved one finger, a perturbation which rapidly stretched the parent muscle was applied. The subjects' task was to return their finger as fast as possible. In a series of identical control experiments, electromyographic activity and performance alone were recorded, but not spindle afferents. Subjects improved their performance by a varying degree when the test was repeated. Optimal performance was usually associated with increased electromyographic activity at a latency of about 60 ms, which was interpreted as a long-latency stretch reflex. The response of the individual spindle afferents to perturbation was uniform in repeated tests regardless of the size of the reflex, e.g. whether it was large or lacking altogether. It was concluded that modulations of the size of the long-latency stretch reflex in the present motor adaptation task were accounted for by mechanisms other than adjustments of the fusimotor activity, because spindle response to an invariant perturbation remained invariant when the size of the reflex varied substantially.

Response profiles of human muscle afferents during active finger movements.

Twenty-five human muscle afferents from the extensor digitorum muscles of the forearm were studied with the microneurographic method. Single unit impulses were recorded while the subjects performed alternating movements of moderate speed at the appropriate metacarpophalangeal joint. For comparison, responses to imposed movements of similar amplitudes and velocities were also studied. Most spindle afferents (n = 17) provided a stretch response with both kinds of movement. However, the impulse rate was slightly higher and the interspike interval variability much larger during active movement. Two units provided deviating response profiles: a flat profile and a converse stretch response. Small and constant torque loads usually failed to modify the response profile but gave rise to a moderate increase of impulse rate in 50% of the spindle afferents. In one single unit, a converse stretch response appeared with opposing loads. Tendon organ afferents (n = 8) were totally unmodulated by imposed stretch in the relaxed muscle. In contrast, their impulse rate was highly modulated during active movements, often following the rectified EMG which resulted in a converse relationship to muscle length and velocity. The findings support the view that, in general, human muscle spindles monitor muscle length and velocity in routine movements of moderate speed as long as opposing loads are small, whereas Golgi tendon organs monitor the amount of muscle recruitment. The significance of the deviating response profiles from spindle afferents remains obscure.

Human muscle spindle response in a motor learning task.

1. Impulse discharge of single muscle spindle afferents from the finger extensor muscles was recorded in the radial nerve of conscious human subjects, during a motor learning task engaging the metacarpo-phalangeal joint of a single finger, using the microneurography technique. 2. Subjects were requested first to pay attention to a complex sequence of imposed single joint movements, and immediately afterwards to reproduce actively the same sequence. No external load was added to the finger and visual control was denied altogether so that subjects relied on mechanoreceptor input exclusively for the sampling and reproduction of movement. In addition, sequences of imposed movements were delivered while subjects were not attending in order to allow analysis of the attention effect. 3. The response of the individual unit was uniform in repeated tests. There were clear differences between spindle firing rate in imposed and actively reproduced movements with most units. However, the difference was complex during the individual sequence, in that firing rate was usually higher during periods of reproduced movements when the muscle was relatively short whereas it was identical when the muscle was relatively long. 4. The hypothesis that reproduction and verification of an imposed movement may be based on simple matching between identical spindle firing in imposed and active movements, was difficult to reject altogether because identical spindle input was present during considerable sections of the movement sequence. It may be speculated that agonists and antagonists cover different ranges of joint excursion, with identical spindle firing rates in imposed and reproduced movements. 5. Attention to imposed movements was associated with a minute and inconsistent increase of spindle firing rate in some afferents and then usually with a slight increase of EMG activity of the parent muscle as well. 6. It was concluded that focusing attention on the kinaesthetic input during imposed movement was not associated with a consistent increase of fusimotor drive.

Role of the human fusimotor system in a motor adaptation task.

1. Single-unit activity was recorded with the microneurographic technique from the radial nerve of attending human subjects. During active finger movements, impulses in spindle afferents from the extensor digitorum muscle were analysed along with joint movements, size of imposed load and EMG activity of the receptor-bearing muscle. 2. In a simple motor adaptation task the subjects were requested to perform ramp-and-hold movements of prescribed amplitudes and velocities at a single metacarpo-phalangeal joint. A test run consisted of a series of movement cycles when the flexor muscle was continuously loaded with a constant torque, immediately followed by cycles when this load was abruptly decreased during the flexion movement, producing a fast stretch of the receptor-bearing muscle. The subjects' task was to strive for movements of constant velocity and particularly to minimize the effect of the disturbance. In order to allow prediction on the basis of immediately preceding cycles, the disturbance was always injected at the same angular position in a number of successive cycles. 3. Motor adaptation was manifested as a successive decrease of the perturbation amplitude, usually associated with the development of a continuous and growing EMG activity in the parent muscle and a growing reflex response of long latency (60 ms). Short-latency reflexes were not seen. 4. The main mechanism accounting for the improved performance was a co-contraction of the agonist-antagonist muscle pair during voluntary movements, producing an increased muscular stiffness. The reflex did not contribute to the motor adaptation because it was not fast enough to curtail the perturbation. 5. The development and the growth of the reflex were not due to a growing fusimotor drive during adaptation, because spindle discharge actually decreased when the reflex increased. The size of spindle response was related to the amplitude of perturbation rather than to the amplitude of the reflex. These findings suggest that reflex modifications were due to central excitability changes which paralleled the muscle contraction. 6. Spindle firing rate during active movements was generally higher in disturbed cycles compared to undisturbed cycles, indicating a higher fusimotor drive. Since muscle contraction was present mainly in the former, this finding may simply represent a case of fusimotor activation along with skeletomotor activation. No indication of an independence between the two was found. 7. The findings lend no support for the view that the size of the stretch reflex in a behavioural task is adjusted by selective changes of the fusimotor drive.