The preferred sensory direction of muscle spindle primary endings influences the velocity coding of two-dimensional limb movements in humans

The present study compares how accurately two different but close velocities of movement are discriminated by populations of muscle spindle primary afferents whether or not one takes into account the direction of the movement and the preferred sensory directions of the units (i.e., the direction of movement to which the afferents are the most sensitive). The activities of 26 muscle spindle primary endings originating from the tibialis anterior, the extensor digitorum longus, the extensor hallucis longus, and the peroneus lateralis muscles were recorded in the lateral peroneal nerve. Their responses to movements imposed at two velocities (12.5 and 18 mm/s) were analyzed. These movements were straight-line movements imposed in eight directions and circular movements in both clockwise and anticlockwise directions. The encoding of the movement velocity was analyzed in two ways. First, the mean frequencies of discharge of the muscle spindle afferents were compared for the two velocities. Second, the data were analyzed using a "neuronal population vector model." This model is based on the idea that such neuronal coding can be analyzed in terms of a series of population vectors (i.e., mean contribution of all the muscle spindle afferents within one directionally tuned muscle) and by finally calculating a sum vector. The results showed no clear and consistent difference in the response frequency of the muscle spindle afferents for the two velocities of movement compared. Rather, the most consistently significant differences between the two velocities were in the lengths of the sum vectors. It is concluded that the encoding of two-dimensional movement velocity relies on populations of muscle spindle afferents coming from the whole set of muscles surrounding a particular joint, each muscle making an instantaneous, oriented, and weighted contribution to the sensory coding of the kinematics parameters.     

Proprioceptive population coding of two-dimensional limb movements in humans: II. Muscle-spindle feedback during "drawing-like" movements

It was proposed to study the proprioceptive sensory coding of movement trajectories during the performance of two-dimensional "drawing-like" movements imposed on the tip of the foot. For this purpose, the activity of the muscle-spindle afferents from the Extensor digitorum longus, Tibialis anterior, Extensor hallucis longus, and Peroneus lateralis muscles was recorded from the lateral peroneal nerve using the microneurographic technique. The drawing movements, describing geometrical shapes such as squares, triangles, ellipses, and circles, were imposed at a constant velocity in both the clockwise and counterclockwise directions. A total number of 44 muscle-spindle afferents were tested, 36 of which were identified as primary and eight as secondary afferents. Whatever the shape of the imposed foot movement, the primary endings from one muscle never discharged throughout the whole trajectory (on average, they discharged for only 49.2% of the length of the trajectory), whereas all the secondary endings discharged for most part of the drawing trajectories (average: 84.8%). The relationship between afferent discharge rate and direction could be described with a cosine-shaped tuning function. The peak of this function corresponded to the preferred sensory direction of the receptor-bearing muscles. The whole path of a given geometrical drawing movement was found to be coded in turn by each of the primary afferents originating from each of the muscles successively stretched. The contribution of each population of muscle afferents from each ankle muscle was represented by a "population vector", whose orientation was the preferred direction of the muscle under consideration and whose length was the mean instantaneous frequency of the afferent population. The "sum vector" corresponding to the sum of all these weighted "population vectors" was found to point in the instantaneous direction of the drawing trajectory, i.e., the tangent to the trajectory. These findings suggest that trajectory information is already encoded at the peripheral level on the basis of the integrated inputs provided by sets of receptors belonging to all the muscles acting on a given joint.     

Proprioceptive population coding of limb position in humans

The present study investigates the coding of positions reached in a two-dimensional space by populations of muscle spindle afferents. The unitary activity of 35 primary muscle spindle afferents originating from the tibialis anterior, extensor digitorum longus, extensor hallucis longus, and peroneus lateralis muscles were recorded from the common peroneal nerve by the microneurographic technique. The steady mean frequency of discharge was analyzed during 16 passively maintained positions of the tip of the foot. These positions were equally distant from and circularly arranged around the "neutral" position of the ankle. The results showed that a same position of the foot was differently coded depending on whether it was maintained for several seconds or whether it was attained after a movement. Muscle spindle activity was increased or decreased, respectively, when the previous movement lengthened or shortened the parent muscle; the magnitude of change in activity depended on the amount of lengthening or shortening in relation to movement direction. Each muscle surrounding the ankle joint was shown to encode the different spatial positions following a directional tuning curve. Data were analyzed by using the "neuronal population vector model". This model consists of calculating population vectors representing the mean contribution of each muscle population of afferents to the coding of a particular position, and by finally calculating a sum vector. The direction of the sum vector was shown to accurately describe the direction of a given maintained position compared to the initial position. We conclude that muscle spindle position coding is based on afferent information coming from the whole set of muscles crossing a given joint. A given spatial position is associated with a stable muscle afferent inflow where each muscle makes an oriented and weighted contribution to its coding. Electronic Publication     

“Proprioceptive signature” of cursive writing in humans: a multi-population coding

The goal of the present study was to investigate the firing behavior of populations of muscle spindle afferents in all the muscles acting on the ankle while this joint was being subjected to writing-like movements. First it was proposed to determine whether the ensemble of muscle spindles give rise to a unique, specific, and reproducible feedback information characterizing each letter, number or short word. Secondly, we analyzed how the proprioceptive feedback on the whole encodes the spatial and temporal characteristics of writing movements using the vector population model. The unitary activity of 51 primary and secondary muscle spindle afferents was recorded in the tibial and common peroneal nerves at the level of the popliteal fossea, using the microneurographic method. The units recorded from belonged to the tibialis anterior, the extensor digitorum longus, the extensor hallucis longus, the peroneus lateralis, the gastrocnemius-soleus and the tibialis posterior muscles. The writing-like movements were randomly imposed at a natural velocity via a computer-controlled machine in a two-dimensional space. In general, muscle spindle afferents from any of the six muscles responded according to the tuning properties of the parent muscle, i.e. increasing their discharge rate during the phases where the direction of movement was within the preferred sensory sector of the parent muscle. The whole trajectory of the writing movements was coded in turn by the activity of Ia afferents arising from all the muscles acting on the joint. Both single afferent responses and population responses were found to be highly specific and reproducible with each graphic sign. The complex multi-muscle afferent pattern involved, with its timing and distribution in the muscle space, seems to constitute a true proprioceptive signature for each graphic symbol. The ensemble of muscle spindle afferents were therefore found to encode the instantaneous direction and velocity of writing movements remarkably accurately. It was concluded that the proprioceptive feedback from all the muscles with which the moving joint is equipped provides the CNS with highly specific information that might contribute to a graphic sign identification process.This work was supported by grants from the Ministère de la Recherche, ACI Cognitique     

Ankle joint movements are encoded by both cutaneous and muscle afferents in humans

We analyzed the cutaneous encoding of two-dimensional movements by investigating the coding of movement velocity for differently oriented straight-line movements and the coding of complex trajectories describing cursive letters. The cutaneous feedback was then compared with that of the underlying muscle afferents previously recorded during the same “writing-like” movements. The unitary activity of 43 type II cutaneous afferents was recorded in the common peroneal nerve in healthy subjects during imposed ankle movements. These movements consisted first of ramp-and-hold movements imposed at two different and close velocities in seven directions and secondly of “writing-like” movements. In both cases, the responses were analyzed using the neuronal population vector model. The results show that movement velocity encoding depended on the direction of the ongoing movement. Discriminating between two velocities therefore involved processing the activity of afferent populations located in the various skin areas surrounding the moving joint, as shown by the statistically significant difference observed in the amplitude of the sum vectors. Secondly, “writing-like” movements induced cutaneous neuronal patterns of activity, which were reproducible and specific to each trajectory. Lastly, the “cutaneous neuronal trajectories,” built by adding the sum vectors tip-to-tail, nearly matched both the movement trajectories and the “muscle neuronal trajectories,” built from previously recorded muscle afferents. It was concluded that type II cutaneous and the underlying muscle afferents show similar encoding properties of two-dimensional movement parameters. This similarity is discussed in relation to a central gating process that would for instance increase the gain of cutaneous inputs when muscle information is altered by the fusimotor drive.     

Cutaneous afferents provide a neuronal population vector that encodes the orientation of human ankle movements

The aim of this study was to analyse the directional coding of two-dimensional limb movements by cutaneous afferents from skin areas covering a multidirectional joint, the ankle. The activity of 89 cutaneous afferents was recorded in the common peroneal nerve, and the mean discharge frequency of each unit was measured during the outward phase of ramp and hold movements imposed in 16 different directions. Forty-two afferents responded to the movements in the following decreasing order (SA2, n = 24/27; FA2, n = 13/17; FA1, n = 3/24; SA1, n = 2/21). All the units activated responded to a specific range of directions, defining their 'preferred sector', within which their response peaked in a given direction, their 'preferred direction'. Based on the distribution of the preferred directions, two populations of afferents, and hence two skin areas were defined: the anterior and the external lateral parts of the leg. As the directional tuning of each population was cosine shaped, the neuronal population vector model was applied and found to efficiently describe the movement direction encoded by cutaneous afferents, as it has been previously reported for muscle afferents. The responses of cutaneous afferents were then considered with respect to those of the afferents from the underlying muscles, which were previously investigated, and an almost perfect matching of directional sensitivity was observed. It is suggested that the common movement-encoding characteristics exhibited by cutaneous and muscle afferents, as early as the peripheral level, may facilitate the central co-processing of their feedbacks subserving kinaesthesia.     

Noise-enhanced kinaesthesia: a psychophysical and microneurographic study

We first explored whether the ability of subjects to detect the direction of slow ramp imposed movements may be improved by the application of mechanical noise to muscle tendons. Movements were plantar/dorsal flexion of the ankle at 0.04°/s, and the amplitude was just sub-threshold for each subject. A white noise signal (random vibration), low-pass filtered to 100 Hz and distributed uniformly in amplitude, was applied to both the extensor and the flexor ankle muscle tendons with four different mean amplitudes (20, 30, 100, 280 μm). The population of subjects was observed to exhibit clear stochastic-type behaviour: their ability to determine the direction of sub-threshold movements significantly increased when the two lower levels of noise were added and subsequently decreased when the noise magnitude was enhanced. Second, using microneurography, we explored the response of 9 primary muscle spindle afferents and 8 cutaneous afferents to the same imposed movements with and without noise application. While these conditions of ankle mobilisation were too small to induce a response in most of the recorded afferents, two muscle afferents exhibited responses that were characteristic of aperiodic stochastic resonance behaviour: the unit movement response was either triggered or improved by the application of an optimal level of noise. All cutaneous afferents were unresponsive to the imposed movements with or without noise application. We conclude that ankle movement sense can be significantly improved by adding an optimal level of mechanical noise to ankle muscle tendons and discuss the optimisation of the response of movement-encoding receptors that may account for this improvement. The application of a mechanical noise on ankle muscle tendons may constitute a means of improving postural stability in subjects with sensory deficits.     

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.     

Ia afferent activity during a variety of voluntary movements in the cat

1. Implanted dorsal root electrodes were used to record discharge trains of single spindle primary afferents (Ia's) of the cat's hind limb during different types of movement.2. The length of the ipsilateral ankle extensors was continuously monitored by an implanted length gauge. Length changes occurring during active stepping were subsequently passively reproduced during brief anaesthesia.3. A comparison of the Ia responses in active and simulated step cycles revealed that moderate fusimotor drive to ankle extensor spindles probably occurred mainly, if not exclusively, during the E(1), E(2) and E(3) phases of active stepping.4. A temporal advance in the Ia response to passive stretching in the F-phase was attributed to the after-effects of fusimotor activity in the extension phases.5. Light thrust applied to the animal's back evoked a potent fusimotor response. This load compensation effect may provide an explanation for the apparently higher degree of alpha-gamma co-activation seen in the mesencephalic locomotor preparation.6. Ankle extensor Ia discharge decreased during falls, despite an increase in extensor e.m.g. This is seen as a clear example of independent alpha and gamma control.7. Placing reactions during walking were consistent with the notion that cutaneous inputs dominate over proprioceptive inputs in these movements.8. alpha and Ia discharge during paw-shaking showed many of the characteristics of that in decerebrate and spastic clonus. The present results suggest that movements resembling clonus may be part of the animal's normal repertoire.9. Isometric co-contraction of agonists and antagonists was found to involve alpha-gamma co-activation.10. Hamstring Ia discharge behaviour during stepping further highlighted the increases in firing rate which normally occur during passive muscle stretching in ;pre-programmed' movements.     

Kinaesthetic role of muscle afferents in man,studied by tendon vibration and microneurography

Summary The characteristics of vibration-induced illusory joint movements were studied in healthy human subjects. Unseen by the subject, constant frequency vibration trains applied to the distal tendon of the Triceps or Biceps induced an almost constant velocity illusory movement of the elbow whose direction corresponded to that of a joint rotation stretching the vibrated muscle. Vibration trains of the same duration and frequency applied alternatively to the Biceps and Triceps evoked alternating flexion-extension illusory movements.During successive application of vibration trains at frequencies from 10 to 120 Hz, the perceived velocity of the illusory movements increased progressively from 10 to 70–80 Hz, then decreased from 80 to 120 Hz. The maximal perceived velocity was three times higher during alternating vibration of the Biceps and Triceps than during single muscle stimulation.Unit activity from 15 muscle spindle primary endings and five secondary endings located in Tibialis anterior and Extensor digitorum longus muscles were recorded using microneurography in order to study their responses to tendon vibration and passive and active movements of the ankle.Primary endings were all activated by low amplitude tendon vibration (0.2–0.5 mm) previously used to induce illusory movements of the elbow. The discharge of some was phase-locked with the vibration cycle up to 120 Hz, while others responded one-to-one to the vibration cycle up to 30–50 Hz, then fired in a sub-harmonic manner at higher frequencies. Secondary endings were much less sensitive to low amplitude tendon vibration.Primary and secondary ending responses to ramp and sinusoïdal movements of the ankle joint were compared. During the movement, the primary ending discharge frequency was almost constant, while the secondary ending activity progressively increased. During ankle movements the primary ending discharge appeared mainly related to velocity, while some secondary activities seemed related to both movement velocity and joint angle position.Muscle spindle sensory ending responses to active and passive ankle movements stretching the receptor-bearing muscle (plantar flexion) were qualitatively and quantitatively similar. During passive reverse movements (dorsiflexion) most of the sensory endings stopped firing when their muscle shortened. Active muscle shortening (isotonic contraction) modulated differently the muscle spindle sensory ending discharge, which could stop completely, decrease or some times increase during active ankle dorsiflexion. During isometric contraction most of the muscle spindle sensory endings were activated.The characteristics of the vibration-induced illusory movements and the muscle spindle responses to tendon vibration and to active and passive joint movements strengthened the possibility of the contribution of primary endings to kinaesthesia, as suggested by several previous works. Moreover, the present results led us to attribute to proprioception in the muscle stretched during joint movement a predominant, but not exclusive, role in this kind of perception.     

Proprioceptive feedback in humans expresses motor invariants during writing

Proprioceptive feedback from populations of muscle spindle afferents feeds the brain with information relating to the instantaneous velocity and direction of ongoing movements. In this paper, we investigate whether the invariant relationship between the velocity and curvature of a trajectory, i.e. the two-thirds power law, is reflected in this muscle spindle feedback. Sixty unitary muscle spindle afferents from six ankle muscle groups were recorded using intraneural microelectrodes during imposed writing-like movements. The movements had kinematic parameters obeying the two-thirds power law and were imposed so that the tip of the foot followed trajectories forming four different letters and six numbers. The responses of the muscle spindle afferent populations were analysed using the population vector model. The results demonstrate that the neuronal trajectories attained from populations of muscle spindles clearly depict the path and kinematic parameters and express the movement invariants, i.e. the trajectory segmentation into units of action and the two-thirds power law. The central vs peripheral origin of such constraints involved in the motor system is discussed.     

The Ia afferent feedback of a given movement evokes the illusion of the same movement when returned to the subject via muscle tendon vibration

The aim of the present study was to further investigate the contribution of primary muscle spindle feedback to proprioception and higher brain functions, such as movement trajectory recognition. For this purpose, complex illusory movements were evoked in subjects by applying patterns of muscle tendon vibration mimicking the natural Ia afferent pattern. Ia afferent messages were previously recorded using microneurographic method from the six main muscle groups acting on the ankle joint during imposed “writing like” movements. The mean Ia afferent pattern was calculated for each muscle group and used as a template to pilot each vibrator. Eleven different vibratory patterns were applied to ten volunteers. Subjects were asked both to copy the perceived illusory movements by hand on a digitizing tablet and to recognize and name the corresponding graphic symbol. The results show that the Ia afferent feedback of a given movement evokes the illusion of the same movement when it is applied to the subject via the appropriate pattern of muscle tendon vibration. The geometry and the kinematic parameters of the imposed and illusory movements are very similar and the so-called “two-thirds power law” is present in the reproduction of the vibration-induced illusory movements. Vibrations within the “natural” frequency range of Ia fibres firing (around 30 Hz) produce clear illusions of movements in all the tested subjects. In addition, increasing the mean frequency of the vibration patterns resulted in a linear increase in the size of the illusory movements. Lastly, the subjects were able to recognize and name the symbols evoked by the vibration-induced primary muscle spindle afferent patterns in 83% of the trials. These findings suggest that the “proprioceptive signature” of a given movement is associated with the corresponding “perceptual signature”. The neural mechanisms possibly underlying the sensory to perceptual transformation are discussed in the general framework of “the neuronal population vector model”.     

Activity patterns in individual hindlimb primary and secondary muscle spindle afferents during normal movements in unrestrained cats.

1. Chronically implanted microelectrode wires in the L7 and S1 dorsal root ganglia were used to record unit activity from cat hindlimb primary and secondary muscle spindle afferents. Units could be reliably recorded for several days, permitting comparison of their activity with homonymous muscle EMG and length during a variety of normal, unrestrained movements. 2. The general observation was that among both primary and secondary endings there was a broad range of different patterns of activity depending on the type of muscle involved and the type of movement performed. 3. During walking, the activity of a given spindle primary was usually consistent among similar step cycles. However, the activity was usually poorly correlated with absolute muscle length, apparently unrealted to velocity of muscle stretch, and could change markedly for similar movements performed under different conditions. 4. Spindle activity modulation not apparently related to muscle length changes was assumed to be influenced by fusimotor activity. In certain muscles, this presumption leads to the conclusion that gamma-motoneurons may be activated out of phase with homonymous alpha-motoneurons as well as by more conventional alpha-gamma-motoneuron coactivation. 5. Simultaneous recordings of two spindle primary afferents from extensor digitorum longus indicated that spindles within the same muscle may differ considerably with respect to this presumed gamma-motoneuron drive. 6. Spindle secondary endings appeared to be predominantly passive indicators of muscle length during walking, but could demonstrate apparently strong fusimotor modulation during other motor activities such as postural changes and paw shaking. 7. Both primary and secondary endings were observed to undergo very rapid modulation of firing rates in response to presumed reflexly induced intrafusal contractions. 8. It is suggested that the pattern of fusimotor control of spindles may be tailored to the specific muscle and task being performed, rather than necessarily dominated by rigid alpha-gamma coactivation.     

Movement detection at the distal joint of the human thumb and fingers

To determine whether proprioceptive acuity is the same at all digits, particularly when postured as in a ’grasp’, we imposed 10° movements at the distal joint of the thumb, index and ring finger, at three velocities; 1.25°/s, 2.5°/s and 5°/s. The test joint was initially flexed by 25° and the joints proximal to the test joint were maintained in a standard posture for each study. When in a grasp posture that disengaged the extensor muscles at the distal joint of the finger, movement detection at the thumb was superior to that at the fingers for all velocities. However, when the fingers were positioned so that all proprioceptive inputs were able to contribute (i.e. cutaneous, joint and both flexor and extensor muscle afferents), proprioceptive acuity was similar for the three digits. Loss of local cutaneous (and joint) inputs by digital anaesthesia significantly impaired performance at all digits, suggesting a critical role for cutaneous input in normal proprioceptive sensibility at all distal joints of the digits. Anaesthesia of the extensor muscle afferents innervating the thumb did not affect its proprioceptive acuity. Thus, for the thumb, the extensor muscle afferents do not provide critical information. The greater change in muscle fascicle length for the thumb’s long flexor muscle (3% per 10°) compared with that in the finger flexor muscles (e.g. 0.1% per 10°) could contribute to the thumb’s performance. There appears to be less redundancy of muscle and non-muscle signals for the fingers than for the thumb, because a reduction in either cutaneous or muscle input significantly impaired acuity at the fingers. Overall, when the hand is in a grasping posture, irrespective of the contribution of local cutaneous inputs, the long flexor acting on the thumb may contribute more to its proprioceptive acuity than the long finger flexors contribute to acuity at the fingers. Received: 20 January 1998 / Accepted:25 March 1998     

Judgment and control of velocity in rapid voluntary movements

Summary Control of velocity in rapid flexion movements of the interphalangeal joint of the thumb was investigated by examining movement trajectories and patterns of activity in the extensor pollicis longus (EPL) and flexor pollicis longus (FPL) muscles. Although velocity was controlled with considerable accuracy, it was not sensed with the same precision. Consistent errors were made when subjects attempted to match the peak velocities under conditions in which the relationship between muscle activity and joint acceleration had been altered, i.e. changing the angle from which movement was initiated or varying the load. Rather than relying on afferent feedback from peripheral sensory receptors for information about velocity during rapid movements, it is suggested that subjects were more likely to base their judgment of velocity on sensations evoked by the voluntary motor command.     

Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study

Summary The activities of single proprioceptive fibres were recorded from the lateral peroneal nerve using transcutaneously implanted tungsten microelectrodes. Unitary discharges originating from muscle spindle primary and secondary endings and Golgi tendon organs were identified by means of various physiological tests. The sensitivity of proprioceptors to mechanical vibrations with a constant low amplitude (0.2–0.5 mm) applied at various frequencies to the tendon of the receptor-bearing muscle was studied. Muscle spindle primary endings (Ia fibres) were found to be the most sensitive to this mechanical stimulus. In some cases their discharge could be driven in a one-to-one manner up to 180 Hz. Most of them also fired harmonically with the vibration up to 80 Hz and then discharged in a subharmonic manner (1/2–1/3) with increasing vibration frequencies. Muscle spindle secondary endings (II fibres) and Golgi tendon organs (Ib fibres) were found to be either insensitive or only slightly sensitive to tendon vibration in relaxed muscles. The effects of tendon vibration on muscle spindle sensory endings response to muscle lengthening and shortening induced by imposed constant velocity or sinusoidal movements of the ankle joint were studied. Modulation of the proprioceptive discharge frequency coding the various joint movement parameters was either completely or partly masked by the receptor response to vibration, depending on the vibration frequency. Moreover, vibrations combined with sinusoidal joint movements elicited quantitatively erroneous proprioceptive messages concerning the movement parameters (amplitude, velocity). The sensitivity of the Golgi tendon organs to vibration increased greatly when the receptor-bearing muscle was tonically contracted. These data confirm that vibration is able to preferentially activate the Ia afferent channel, even when the vibration amplitude is low. They define the frequency sensitivity of the muscle spindle primary and secondary endings and the Golgi tendon organs. They also show that the physiological messages triggered by ongoing motor activities undergo a series of changes during the exposure of muscles to vibration.     

Afferent mechanisms for the reflex response to imposed ankle movement in chronic spinal cord injury

We have reported earlier that externally imposed ankle movements trigger ankle and hip flexion reflexes in individuals with spinal cord injury (SCI). In order to examine the afferent mechanisms underlying these movement-triggered reflexes, controlled ankle movements were imposed in 17 SCI subjects. In 13 of these subjects, reflex torques were recorded at the hip, knee and ankle in response to 5 ankle movement ranges, and 4 movement speeds. Subjects were tested using both ankle plantarflexion and dorsiflexion movements. The principal outcome measure, peak hip flexion torque of the induced reflexes, was used for comparing the effects of movement range and speed on the reflex response. We found that movement-triggered reflexes were sensitive to the angular range of ankle deflection, but insensitive to the velocity of the movement. Movement amplitudes sufficient to trigger hip and ankle flexion were routinely associated with increases in ankle passive force, suggesting that force-sensitive receptors participated in the reflex response. However, increases in angular range also corresponded to increases in muscle length, making it difficult to distinguish whether the response was triggered by a load-sensitive receptor (e.g., Golgi tendon organ or muscle free nerve ending) or a position-sensitive receptor responsive to absolute ankle angle (e.g., muscle spindle secondary afferent). The absence of velocity dependence of the reflex suggested that spindle Ia afferents were not major contributors. These results suggest movement-triggered reflexes originate in muscle receptors that are sensitive to either absolute muscle length, to muscle force or to both. Although receptors that are sensitive to absolute muscle length cannot be excluded with certainty, the finding that reflex responses require that ankle movements elicit an increase in passive force argues for a prominent role of nonspindle mechanoreceptors, such as group III/IV muscle afferents. These afferents are activated preferentially as muscles are stretched to near maximum length, and they appear to have potent reflex effects in spinal cord injury.     

Three-dimensional sensitivity and caudal projection of neck spindle afferents

1. We recorded from neck muscle spindle afferents in the C2 dorsal root ganglion of the decerebrate cat using floating electrodes. The afferents presumably innervated mainly ventral and ventrolateral perivertebral muscles, and sternocleidomastoid. Stimuli consisted of combinations of rotatory head movements about the roll/pitch or pitch/yaw axes. An important difference from our earlier experiments (10) was the addition of yaw movement to the stimulus paradigm making possible a three-dimensional analysis of afferent behavior. 2. For each afferent we determined the most effective direction of tilt (orientation of the response vector) in three dimensions by using sinusoidal stimuli that combined pitch and roll, or pitch and yaw, or by measuring the gains to responses to roll, pitch, and yaw rotation. 3. Most afferents were sensitive to rotation around all three axes; pitch and yaw were usually more effective than roll. There was no indication of clustering of response vectors, as might be expected if the receptors were located in a small number of muscles each of which has receptors aligned in a homogeneous direction. 4. The responses of afferents were further studied using sinusoidal and trapezoidal stimuli aligned as closely as possible with the orientation of their response vector. The availability of the yaw stimulus made receptor classification based on response linearity, gain, and dynamic index more reliable than in our earlier experiments (10). 5. Muscle spindle responses were divided into three categories: A, B, and ambiguous. The evidence suggests that category A are probably spindle primary receptors and category B are secondaries. Ambiguous receptors have intermediate properties. 6. The caudal projection of spindle afferents was examined by delivering antidromic stimuli with a movable electrode on the surface of the ipsilateral dorsal column. Eighteen percent of the afferents projected to C4, and 14% as far as C5. Long caudal projections can be found in A, B, and ambiguous receptors with a range of directional sensitivities. 7. The evidence suggests that C2 spindle afferents make synapses in the midcervical segments with interneurons and propriospinal neurons that are part of the intraspinal pathway of the tonic neck reflex.     

Local subcutaneous and muscle pain impairs detection of passive movements at the human thumb

Activity in both muscle spindle endings and cutaneous stretch receptors contributes to the sensation of joint movement. The present experiments assessed whether muscle pain and subcutaneous pain distort proprioception in humans. The ability to detect the direction of passive movements at the interphalangeal joint of the thumb was measured when pain was induced experimentally in four sites: the flexor pollicis longus (FPL), the subcutaneous tissue overlying this muscle, the flexor carpi radialis (FCR) muscle and the subcutaneous tissue distal to the metacarpophalangeal joint of thumb. Tests were conducted when pain was at a similar subjective intensity. There was no significant difference in the ability to detect flexion or extension under any painful or non-painful condition. The detection of movement was significantly impaired when pain was induced in the FPL muscle, but pain in the FCR, a nearby muscle that does not act on the thumb, had no effect. Subcutaneous pain also significantly impaired movement detection when initiated in skin overlying the thumb, but not in skin overlying the FPL muscle in the forearm. These findings suggest that while both muscle and skin pain can disturb the detection of the direction of movement, the impairment is site-specific and involves regions and tissues that have a proprioceptive role at the joint. Also, pain induced in FPL did not significantly increase the perceived size of the thumb. Proprioceptive mechanisms signalling perceived body size are less disturbed by a relevant muscle nociceptive input than those subserving movement detection. The results highlight the complex relationship between nociceptive inputs and their influence on proprioception and motor control.