Unmyelinated tactile afferents signal touch and project to insular cortex.

There is dual tactile innervation of the human hairy skin: in addition to fast-conducting myelinated afferent fibers, there is a system of slow-conducting unmyelinated (C) afferents that respond to light touch. In a unique patient lacking large myelinated afferents, we found that activation of C tactile (CT) afferents produced a faint sensation of pleasant touch. Functional magnetic resonance imaging (fMRI) analysis during CT stimulation showed activation of the insular region, but not of somatosensory areas S1 and S2. These findings identify CT as a system for limbic touch that may underlie emotional, hormonal and affiliative responses to caress-like, skin-to-skin contact between individuals.

Proprioceptive feedback is reduced during adaptation to a visuomotor transformation: preliminary findings.

Adapting movements in relation to visual feedback is a ubiquitous characteristic of sensorimotor control and involves the integration of multiple sources of sensory information. We recorded sensory feedback from muscle spindle afferents during visuomotor adaptation while subjects performed an aiming task to investigate whether the activity of the muscle spindles was modulated by the fusimotor system under these learning conditions. None of the muscle spindles showed an increase in activity, rather in 83% of the trials the firing rates were decreased. These preliminary results suggest that the CNS reduces the sensory signals arising from muscle spindles perhaps as a means of resolving the conflict between visual and proprioceptive feedback during the task.

Directional tuning of human forearm muscle afferents during voluntary wrist movements.

1. Single unit activity was recorded with the microneurography technique from sixteen spindle afferents and one Golgi tendon organ afferent originating from the forearm extensor muscles. Impulse rates were studied while subjects performed unobstructed aiming movements at the wrist in eight different directions 45 deg apart. In addition, similar imposed movements were performed while the subject was instructed to remain relaxed. Movement amplitudes were about 5 deg and the speed 10-30 deg x s(-1). Joint movements were translated to movements of a cursor on a monitor to provide visual feedback. 2. Individual spindle afferents modulated their activity over a number of targets, i.e. were broadly tuned, during these aiming movements. The preferred direction for a spindle afferent was the same during both passive and active movements, indicating that the fusimotor effects associated with active contractions had little or no effect on the direction of tuning. 3. The direction of tuning of individual spindle afferents could be predicted from the biomechanically inferred length changes of the parent muscle. Thus spindle afferents responded as stretch receptors, i.e. impulse rates increased with lengthening and decreased with shortening, in active as well as passive movements. 4. Spindles from muscles, which continuously counteracted gravity exhibited a stretch response and directional tuning during the phase of movement alone whereas their position sensitivity was poor. In contrast, spindle afferents from the muscles that had no or minimal antigravity role were directionally tuned during both the dynamic and the static phase of the aiming task and their position sensitivity was substantially higher. 5. In spite of the limited data base from three extensor muscles it could be demonstrated that wrist joint position was remarkably well encoded in the ensemble muscle spindle data. In some cases the ensemble muscle spindle data encoded the instantaneous trajectory of movement as well.

Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin.

Impulses were recorded from unmyelinated afferents innervating the forearm skin of human subjects using the technique of microneurography. Units responding to innocuous skin deformation were selected. The sample (n = 38) was split into low-threshold units (n = 27) and high-threshold units (n = 11) on the basis of three distinctive features, i.e., thresholds to skin deformation, size of response to innocuous skin deformation, and differential response to sharp and blunt stimuli. The low-threshold units provisionally were denoted tactile afferents on the basis of their response properties, which strongly suggest that they are coding some feature of tactile stimuli. They exhibited, in many respects, similar functional properties as described for low-threshold C-mechanoreceptive units in other mammals. However, a delayed acceleration, not previously demonstrated, was observed in response to long-lasting innocuous indentations. It was concluded that human hairy skin is innervated by a system of highly sensitive mechanoreceptive units with unmyelinated afferents akin to the system previously described in other mammals. The confirmation that the system is present in the forearm skin and not only in the face area where it first was identified suggests a largely general distribution although there are indications that the tactile C afferents may be lacking in the very distal parts of the limbs. The functional role of the system remains to be assessed although physiological properties of the sense organs invite to speculations that the slow tactile system might have closer relations to limbic functions than to cognitive and motor functions.

Is human muscle spindle afference dependent on perceived size of error in visual tracking?

Impulses of 16 muscle spindle afferents from finger extensor muscles were recorded from the radial nerve along with electromyographic (EMG) activity and kinematics of joint movement. Twelve units were classified as Ia and 4 as II spindle afferents. Subjects were requested to perform precision movements at a single metacarpophalangeal joint in an indirect visual tracking task. Similar movements were executed under two different conditions, i.e. with high and low error gain. The purpose was to explore whether different precision demands were associated with different spindle firing rates. With high error gain, a small but significantly higher impulse rate was found in pooled data from Ia afferents during lengthening movements but not during shortening movements, nor with II afferents. EMG was also significantly higher with high error gain in recordings with Ia afferents. When the effect of EMG was factored out, using partial correlation analysis, the significant difference in Ia firing rate vanished. The findings suggest that fusimotor drive as well as skeletomotor activity were both marginally higher when the precision demand was higher, whereas no indication of independent fusimotor adjustments was found. These results are discussed with respect to data from behaving animals and the role of fusimotor independence in various limb muscles proposed.

Pulsatile motor output in human finger movements is not dependent on the stretch reflex.

1. Stretch perturbations were delivered during slow voluntary finger movements with the aim of exploring the role of the stretch reflex in generating the 8-10 Hz discontinuities that characterize these movements. Afferent activity from muscle spindle primary endings in the finger extensor muscles was recorded from the radial nerve, along with the EMG activity of these muscles, and kinematics of the relevant metacarpo-phalangeal joint. 2. Perturbations elicited a distinct response from the muscle spindles appearing at the recording electrode after 13 ms, and weak reflex responses from the muscle with peak values at 53 and 63 ms during flexion and extension, respectively. 3. The time relations between kinematics, spindle firing and modulations of EMG activity elicited by the perturbations were compared with those of the self-generated discontinuities. These analyses indicate that stretch reflex mechanisms cannot account for the modulations of EMG activity that give rise to successive 8-10 Hz discontinuities. 4. A comparison of the reflex responses to perturbations with the EMG modulations during self-generated movements indicates that the reflex was too weak to account for the pulsatile motor output during voluntary movements. 5. By inference it was concluded that the 8-10 Hz discontinuities during self-generated movements are probably generated by mechanisms within the central nervous system.

Fusimotor and skeletomotor activities are increased with precision finger movement in man.

1. Impulses of eighteen muscle spindle afferents from finger extensor muscles were recorded from the radial nerve while subjects performed single joint finger movements of two kinds, i.e. routine and precision, which were nearly identical with regard to kinematics. 2. The firing rates of ten primary and two secondary spindle afferents were higher in the precision movements by more than 10%, although the difference reached statistical significance in only seven of them. In most cases when spindle firing was higher in precision movements the skeletomotor activity was higher as well. 3. The findings indicated that the fusimotor activity was often stronger with precision movements compared with routine movements. This result is in qualitative agreement with several studies on behaving cats, demonstrating higher fusimotor activity in more demanding motor tasks. On the other hand, the effects were much smaller in humans than in cats. Moreover, in contrast to findings from experiments in cats, no support was obtained for the hypothesis that fusimotor activity was adjusted independently of the skeletomotor activity in human finger muscles.

Coding of pulsatile motor output by human muscle afferents during slow finger movements.

1. Impulse activities of thirty-eight muscle spindle and tendon organ afferents from the finger extensor muscles were recorded in the radial nerve of human subjects while the subjects performed voluntary flexion and extension finger movements at a single metacarpophalangeal joint. 2. The afferent firing was analysed in relation to the 8-10 Hz discontinuities which previously have been shown to characterize these movements. Spike-triggered averaging and frequency domain analyses demonstrated that all Ia muscle spindle afferents and a large proportion of group II spindle afferents responded in close association with local peaks in the joint acceleration. During muscle lengthening the impulses appeared during phases of rapid muscle stretch, whereas they appeared during the phase of minimal speed during muscle shortening. 3. The Golgi tendon organ (Ib) afferents displayed a reverse pattern of activity in relation to the discontinuities, i.e. the impulses tended to appear in the phase of minimal speed during lengthening movements and close to maximal shortening speed during shortening movements. Hence, their firing often coincided with the phasic increases of the parent muscle activity which account for the 8-10 Hz discontinuities. 4. A close analysis of the time relations between spindle firing and the kinematics of the 8-10 Hz discontinuities revealed that the population spindle response was too delayed and too dispersed to support the hypothesis that the discontinuities are accounted for by the stretch reflex. 5. If, as suggested in a previous paper, the 8-10 Hz discontinuities are produced by a pulsatile descending motor command, the coding of the periodic but tenuous kinematic events by the population of proprioceptors may have a role in relation to an alleged pulsatile command generator.

Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects.

1. Impulses in single nerve fibres from the lateral antebrachial cutaneous nerve were recorded using the microneurography technique in human subjects. 2. In a sample of fifty-five mechanoreceptive units with fast-conducting nerve fibres, five types were identified, i.e. SAI (slowly adapting type I, Merkel), SAII (slowly adapting type II, Ruffini), hair units, field units and Pacinian-type units. The latter three unit types were all rapidly adapting. 3. The detailed structure of thirty-five receptive fields of SAI, SAII, hair and field units was explored with a method which was objective and independent of the experimenter's skill and experience. A lightweight probe was used to scan the receptive field area in a series of tracks 0.23 mm apart while single-unit activity was recorded. 4. SAI fields were small and composed of two to four well-separated high-sensitivity spots and often, in addition, one minor spot of lower sensitivity. SAII units typically fired spontaneously at a low and regular rate. Most fields consisted of one single spot of high sensitivity with diffuse borders. The hair units innervated ten to thirty-three (or more) hairs, which were evenly distributed over a large area. The field units were characterized by a number of small and closely packed high-sensitivity spots with diffuse borders. A conservative estimate indicated eleven spots per unit. 5. The findings indicate that the sheet of mechanoreceptors on the skin of the forearm is distinctly different from that on the dorsum of the hand and in the face. It seems reasonable to assume that the former is more representative for the hairy skin covering the main parts of the body.

Human muscle spindle afferent activity in relation to visual control in precision finger movements.

1. Impulse activities of muscle spindle afferents from the finger extensor muscles were recorded in the radial nerve of human subjects. In addition to single unit activity, surface EMG was recorded as well as finger joint position and angular velocity. 2. All units were studied under two conditions of voluntary finger movements. In the visual condition, the subject tracked ramp and hold sequences at a single metacarpophalangeal joint. In the non-visual condition the subject was asked to produce the same movement while visual control was denied altogether. 3. With sixteen units, detailed statistical analyses failed to reveal significant differences in muscle spindle afferent activity between the visual and the non-visual task. However, with two group Ia units, impulse rate was marginally but significantly higher in the visual task even when differences in average movement velocity, velocity variability and EMG level had been factored out. 4. The findings suggested that access to visual information for movement control did not produce any large-scale differences in spindle afference, although a small effect of an increased and independent gamma-activation emerged in the statistical analysis in 11% of the units.

The discharge behaviour of single vasoconstrictor motoneurones in human muscle nerves.

1. The discharge behaviour of fourteen single sympathetic vasoconstrictor efferents was studied using a tungsten microelectrode inserted percutaneously into a motor fascicle of the radial or peroneal nerve in eight awake supine subjects. Units were classified as vasoconstrictor because their firing properties correlated appropriately to changes in cardiac interval and arterial pressure. 2. On average, individual vasoconstrictor units discharged in only 21% of heart beats, with an overall mean frequency of 0.47 Hz. Usually only one spike was generated per cardiac cycle. Calculated from cardiac cycles in which a unit fired from two to seven spikes, the mean within-burst firing rate was 18.8 +/- 2.5 Hz (mean +/- S.E.M.); but instantaneous frequencies above 50 Hz were occasionally observed. 3. Measured from a defined R-wave of the ECG, the spike onset latency varied over 358 +/- 33 ms, suggesting considerable variation of synaptic delays in the baroreflex arc. This latency had a relatively uniform temporal relationship with the burst onset or peak latency, compatible with a fixed recruitment order of individual sympathetic neurones. 4. In view of the low average firing rate of individual units we suggest that the variable instantaneous firing rates may optimize the contractile responses of vascular smooth muscle.

A system of unmyelinated afferents for innocuous mechanoreception in the human skin.

It is generally held that tactile mechanisms in the human skin are served by fast-conducting myelinated nerve fibres, whereas touch-sensitive afferents with unmyelinated axons are lacking in man, in contrast to other mammals. In the present study we found evidence that sensitive mechanoreceptive afferents with unmyelinated fibres are quite common and widespread in the hairy skin of human subjects. Their biological role remains an enigma which might attract more attention now that their existence in man has been demonstrated.

Organization of motor output in slow finger movements in man.

1. Slow finger movements were analysed in normal human subjects with regard to kinematics and EMG activity of the long finger muscles. Surface EMG from the finger extensor and flexor muscles on the forearm was recorded along with angular position and angular velocity during voluntary ramp movements at single metacarpophalangeal joints. Angular acceleration was computed from the velocity record. 2. It was found that movements were not smooth but characterized by steps or discontinuities, often recurring at intervals of 100-125 ms, yielding velocity and acceleration profiles dominated by 8-10 Hz cycles. The discontinuities were manifest from the very first trial and thus not dependent on training. Their amplitude and amount varied between subjects but were relatively stable for the individual subject. 3. The 8-10 Hz cycles were seen with voluntary ramp movements of widely varying velocities, higher velocities being associated with larger steps recurring with the same repetition rate as the small steps of slow voluntary ramps. Maximal step amplitude observed was more than one order of magnitude larger than physiological tremor. 4. The individual 8-10 Hz cycle was asymmetrical in that decelerations usually reached higher peaks than the preceding acceleration, suggesting that the antagonist contributed with a braking action. Moreover, in very slow voluntary ramps, the movement cycles were often interspaced by periods of zero velocity, providing a highly non-sinusoidal velocity profile. 5. The EMG of the agonist and the antagonist muscles was modulated in close relation to the accelerations and decelerations respectively of the individual movement cycle. These modulations were present in both extensor and flexor muscles, although they were more consistent and usually more prominent in the former. 6. The findings indicate that a feature of slow finger movements was an 8-10 Hz periodic output to the muscular system, suggesting that slow finger movements are implemented by a series of biphasic force pulses, involving not only the shortening agonist muscle propelling the movement, but the antagonist muscle as well whose activity increased shortly after the agonist and contributed to a sharp deceleration of the individual step of movement. 7. It is proposed, as a hypothesis, that this biphasic motor output may reflect a similar organization of the descending motor command for slow finger movements. Hence, this command would include a series of biphasic pulses, concatenated at a rate of 8-10 per second and a pulse-height regulator capable of setting the size of the pulse and thus the overall speed of the movement.

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.

Muscle afferent responses to isometric contractions and relaxations in humans.

1. One hundred and two single afferents from the finger extensor muscles of humans were studied with the microneurography technique. 2. The afferents were provisionally classified as primary muscle spindle afferents (62/102), secondary spindle afferents (22), and Golgi tendon organ afferents (18) on the basis of their responses to four tests: 1) ramp-and-hold stretch, 2) 20- and 50-Hz small-amplitude sinusoidal stretch superimposed on ramp-and-hold stretch, 3) maximal isometric twitch contraction, and 4) stretch sensitization. 3. The response profiles of the three unit types were analyzed during slowly rising isometric contraction terminating with an abrupt relaxation. About 75% (61/84) of all muscle spindle afferents increased their discharge during isometric contraction, whereas the discharge was reduced for the remaining afferents. All Golgi tendon organs increased their discharge during the contraction. 4. The level of extrafusal contraction at which a spindle afferent increased its discharge rate often varied from trial to trial, speaking against a fixed fusimotor recruitment level of the individual spindle ending. 5. In 70% of the spindle afferents, a distinct burst of impulses appeared when the subject rapidly relaxed after the isometric contraction. The burst was more common and usually much more prominent with primary than secondary afferents, often reaching instantaneous discharge rates well above 100 Hz. 6. Whereas all Golgi tendon organ afferents displayed an increased discharge during the contraction phase, only one of them exhibited a rate acceleration close to the relaxation phase. However, this response could clearly be identified as being of different nature than the spindle bursts.(ABSTRACT TRUNCATED AT 250 WORDS)

Classification of human muscle stretch receptor afferents: a Bayesian approach.

1. A sample of 124 human muscle afferents originating from the finger extensor muscles were recorded from the radial nerve in the upper arm. A method is described to formalize the classification of units in muscle spindle primary and secondary afferents and Golgi tendon organ afferents on the basis of a few, nonrigorous assumptions. The classification was based on experimental data that largely have been described in a series of previous papers, although some additional data were collected in the present study. 2. The units were subjected to five tests providing identification data: twitch contraction test, ramp-and-hold stretch, small-amplitude sinusoidal stretches superimposed on ramp stretch, stretch sensitization, and isometric contraction/relaxation. From these five tests the following eight response features were extracted: response to maximal isometric twitch contractions, type of stretch sensitization, correlation between discharge rate and contractile force, response to sudden isometric relaxation, presence or absence of an initial burst, deceleration response, prompt silencing at slow muscle shortening, and driving by small-amplitude sinusoidal stretches. 3. A Bayesian decision procedure was adopted to classify the units on the basis of the eight discriminators. As a first step, units were provisionally classified into muscle spindle primary and secondary afferents, and Golgi tendon organ afferents, by intuitively weighting their responses to the identification tests. Prior probabilities were estimated on the basis of the provisional classification. The eight response features were analyzed and tabulated for all afferents, and the likelihood functions of the tests were directly calculated on the basis of these data.(ABSTRACT TRUNCATED AT 250 WORDS)