Structure And Response Properties Of Proprioceptors

There are several reviews in the literature on the morphology and response properties of mechanoreceptors that signal locomotor movements (vertebrates: Granit 1970; Matthews 1972; Hulliger 1984; Prochazka 1989; Johansson et al. 1991; Jami 1992; Prochazka 1996b; Prochazka and Gorassini 1998a; Prochazka 1999; invertebrates: Bassler 1983; French 1988; Burrows 1992; Bassler and Buschges 1998). In the following, we will concentrate mainly on mammalian proprioceptors, muscle spindles, and tendon organs.

6.5.1 Muscle Spindles: Structure

There are 25,000-30,000 muscle spindles in the human body, including about 4000 in each arm and 7000 in each leg (Voss 1971; Hulliger 1984). The average number of spindles in a mammalian muscle is roughly 38*(cube root of mass in grams) (Banks and Stacey 1988; Prochazka 1996b). Thus a 64 g muscle contains about 152 spindles. On average, a single limb muscle in the cat contains 50 to 200 spindles, each ranging from 2 mm to 6 mm in length (Voss 1971; Boyd and Gladden 1985). A muscle spindle consists of a dozen or so intrafusal muscle fibers (Latin "fusus" = spindle) attached at each end to the surrounding extrafusal muscle fiber, with a central region innervated by sensory endings encased in a capsule (Boyd and Gladden 1985). The spindle lengthens and shortens along with the extrafusal muscle fibers to which it is attached. The typical spindle in cats, monkeys, and humans contains three types of intrafusal muscle fiber: a dynamic bagj (DB1 or bj), a static bag2 (SB2 or b2), and 2-11 chain (c) fibers. These intrafusal fibers receive motor input from 10-12 fusimotor axons and sometimes from a P-skeletofusimotor axon, which also innervates neighboring extrafusal muscle fibers (Emonet-Denand et al. 1975; Hulliger 1984; Banks 1994). The central encapsulated region of the spindle contains 1 primary and up to 5 secondary sensory endings spiraled around the non-contractile portions of the intrafusal fibers (Boyd and Gladden 1985). The primary endings are those of group Ia afferents (conduction velocity 72-120 m/s in cats) and the secondary endings are those of group II afferents (20-72 m/s) (Matthews 1972).

6.5.2 Passive Response Properties of Spindle Afferents

Spindle primary and secondary endings respond to muscle length variations similarly in cats, monkeys, and humans (for detailed comparisons and a discussion of scaling for different muscle lengths see Prochazka 1981; Prochazka and Hulliger 1983). In the absence of fusimotor action, group Ia and II afferents respond to muscle length changes dynamically, Ia afferents being more sensitive to muscle velocity and acceleration (e.g., they respond to ramp stretches with larger jumps in firing rate and they show more phase advance in response to sinusoidal inputs). There is a continuum from the smallest diameter group II afferents with low velocity sensitivity, to the largest diameter Ia afferents with high velocity- and acceleration-sensitivity. Group Ia and II afferents both have non-linear aspects of response: e.g., stretch sensitivity that depends on amplitude and offset, after-effects of muscle and fusimotor contraction and non-linear velocity scaling (Hulliger 1984; Prochazka 1996b).

6.5.3 Fusimotor Action

The b1 fiber and its associated Ia sensory spirals are selectively activated by dynamic fusimotor (ad) or Pd skeletofusimotor axons (Boyd and Gladden 1985; Boyd et al. 1985; Banks 1994). The b2 and chain fibers are activated by static fusimotor or skeletofusimotor (as or Ps) axons and rarely by ad or Pd axons (Banks et al. 1998). Up to 30% of hindlimb spindles lack b1 fibers and their group Ia afferents are then called b2c afferents (Boyd and Gladden 1985; Taylor et al. 1992; Taylor et al. 1998; Taylor et al. 1999).

The main fusimotor actions can be summarized as follows. When muscle length changes are small (< 0.5% rest length), pure ad action, mediated by b1 fibers, increases the background firing rate (bias), decreases the stretch-sensitivity (gain) and reduces the phase advance of group Ia afferents (Emonet-Denand et al. 1977). For larger-amplitude length changes, ad action increases group Ia stretch-sensitivity up to five-fold (Boyd et al. 1985) and either increases or decreases Ia phase advance slightly (Hulliger et al. 1977; Chen and Poppele 1978). Type b2c Ia afferents do not exhibit dynamic fusimotor effects, the b1 intrafusal fibers being absent. as action strongly increases the bias of both group Ia and II sensory endings and reduces group Ia stretch sensitivity (gain) by 50% or more for all amplitudes of length change (Cussons et al. 1977; Chen and Poppele 1978). Paradoxically, weak as action can increase Ia gain (Hulliger et al. 1985). In either case, phase is little changed. Of the 6 to 9 as axons acting on a group II ending, each produces some bias, most attenuate its sensitivity to small stretches (< 1% rest length) but one or two of the as axons substantially increase group II sensitivity to stretches, presumably by activating b2 intrafusal fibers (Jami and Petit 1978). The sensitizing action of these as fibers on group II endings is similar to the action of ad fibers on Ia endings. The terms dynamic and static fusimotor action are in fact misleading, in that both types alter mainly the gain and offset rather than the dynamics of group Ia and II responses to stretch (Prochazka 1996b).

6.5.4 Spindle Models

Mathematical models of spindle response characteristics were originally developed from results obtained in acute experiments (Matthews and Stein 1969; Poppele and Bowman 1970; Poppele and Kennedy 1974; Chen and Poppele 1978; Poppele 1981). These models have recently been tested and compared in ensembles of group Ia and II afferent activity recorded in freely moving cats (Prochazka and Gorassini 1998a; Prochazka and Gorassini 1998b). Because all of the Ia models have a velocity-sensitive term and this tends to dominate the response to the relatively fast changes in muscle length that occur in locomotion, most of the models were reasonably successful in predicting the group Ia responses from the muscle length and EMG activity profiles, as exemplified in the ensemble firing profile of hamstrings Ia afferents shown in Figure 6.1. In this example, the small EMG term was added to provide a small amount of alpha-linked biasing of the Ia firing rate, to represent alpha-gamma linkage. In both the group Ia and II models, fusimotor action is usually represented as a single gain parameter though a more comprehensive model has been developed that incorporates some of the non-linear features of fusimotor action (Schaafsma et al. 1991; Otten et al. 1995). Modelling has provided some crucial insights into locomotor control in recent years and the mathematical models of spindle and tendon organ responses have played an important role in this.

6.5.5 Tendon Organs: Structure and Response Properties

Tendon organs are encapsulated structures 0.2-1 mm long, usually located at musculotendinous junctions (Barker 1974). Generally speaking, there are about 80% as many tendon organs in a typical limb muscle as spindles. Their sensory endings, which become group Ib afferent axons, are entwined among the tendinous strands of 10-20 motor units, a given motor unit affecting 1-6 tendon organs (Proske 1981; Jami 1992). The sensory endings are compressed when the tendon is put under tensile stress. When non-contracting muscles are stretched, the force transmitted by the tendon is low except at the extreme end of the physiological range. Because many tendon organs only fire significantly at such extremes, it was initially posited that they were overload protectors. It was then found that their sensitivity to force changes produced by activating selected motor units was much higher than to force changes produced by passive stretch of the whole muscle (Houk and Henneman, 1967). This led to the idea that they were more sensitive to active force than to passive force. However when their force-sensitivity was compared in active contractions and passive stretching of the whole muscle, no significant difference was found (Stuart et al. 1970, Stephens et al. 1975).

FIGURE 6.1 Ensemble firing profile of 9 hamstrings spindle primary (group Ia) afferents recorded during overground locomotion in normal cats. Top: muscle length, middle: elec-tromyogram (EMG), bottom: firing rate profile with superimposed predicted rate derived from the length and EMG signals. Reprinted from Prochazka, A., Prog. Brain Res, ©1999. pp. 133-142, with permission from Elsevier Science.

FIGURE 6.1 Ensemble firing profile of 9 hamstrings spindle primary (group Ia) afferents recorded during overground locomotion in normal cats. Top: muscle length, middle: elec-tromyogram (EMG), bottom: firing rate profile with superimposed predicted rate derived from the length and EMG signals. Reprinted from Prochazka, A., Prog. Brain Res, ©1999. pp. 133-142, with permission from Elsevier Science.

6.5.6 Tendon Organ Models

Because it is impossible to monitor the net force produced by the particular group of motor units "sampled" by a tendon organ, it is difficult to determine precise input/output characteristics for the receptor. Nonetheless, frequency analyses have © 2002 CRC Press LLC

been performed by applying feedback-controlled force signals to the whole muscle (Houk and Simon 1967; Anderson 1974; Stephens et al. 1975). These showed that tendon organs had transfer functions comparable to those of spindle group II endings (Alnaes 1967). Like group II afferents, tendon organ group Ib afferents fire fairly regularly, except at very low levels of active force, when unfused twitch contractions of newly recruited motor units may cause bursts of group Ib firing (Jami et al. 1985). Various types of non-linearity in tendon organ transduction have been described. For example, a given Ib ending may be unloaded by contractions of muscle fibers not inserting into the receptor capsule (Houk and Henneman 1967; Stuart et al. 1972). As group Ib afferents sample from a restricted subset of motor units, they do not necessarily signal whole muscle force linearly (Jami et al. 1985). The transfer function models describing the relationship between whole muscle force and Ib firing rate (Houk and Simon 1967; Anderson 1974) have recently been tested on firing profiles of small ensembles of Ib afferents recorded during locomotion in normal cats. The EMG activity from the receptor-bearing muscles was used in lieu of muscle force. In spite of this substitution, and in spite of concomitant length changes which would have modulated force somewhat due to inherent force-length properties of the muscles, the tendon organ firing rate profiles were surprisingly well predicted (Figure 6.2).

6.5.7 Mechanoreceptors in Joints, Ligaments, and Skin

Mechanoreceptors in joint capsules, joint ligaments, and skin are strategically placed to provide proprioceptive feedback, but proving this role has been difficult. Until the late 1960s, joint receptors were assumed to signal joint position over the full range of motion (Boyd and Roberts 1953). However, it was then reported that most joint receptors in the cat knee and wrist only fired at the extremes of the range (Burgess and Clark 1969; Tracey 1979). Subsequently, several groups reported full-range signaling (Godwin-Austen 1969; Zalkind 1971; Carli et al. 1979; Ferrell 1980; Lund and Matthews 1981) though some of the full-range afferents in the cat knee joint may have been either muscle spindle or tendon organ afferents (McIntyre et al. 1978). Loading of the joint capsule by muscle contraction sensitizes joint receptors, in some cases enough to confer mid-range responsiveness on them (Grigg and Greenspan 1977).

On balance, it seems that joint capsular and ligamentous afferents are capable of signaling limb position and movement at the extremes of motion and in some joints over the full range of motion. Single-unit discharges are detectable in recordings from whole joint nerves (Ferrell 1980), so the total number of joint receptors signaling mid-range movement is probably low compared to the number of muscle and skin receptors responding to the same movement. Joint afferents have conduction velocities mainly in the group II range (Burgess and Clark 1969) and their segmental reflex connections with a-motoneurons are less direct than those of muscle spindles (Johansson et al. 1991; Jankowska 1992). It has been suggested that they have a special role in reflexly inhibiting motoneurons of muscles near joints that are damaged (Iles et al. 1990).

Cutaneous receptors overlying joints and muscle respond phasically as well as tonically to movement (Edin and Abbs 1991; Edin 1992; Edin and Johansson 1995;

FIGURE 6.2 Ensemble firing profile of 4 triceps surae tendon organ (group Ib) afferents recorded during overground locomotion in normal cats. A. Top: muscle length, second panel: electromyogram (EMG), third panel: ensemble Ib firing rate profile with superimposed predicted rate derived from the EMG signal, B: muscle force as predicted from the firing rate, C: mean force in soleus obtained in separate experiments in another laboratory (Herzog et al. 1993). Reprinted from Prochazka, A., Prog. Brain Res, ©1999. pp. 133-142, with permission from Elsevier Science.

FIGURE 6.2 Ensemble firing profile of 4 triceps surae tendon organ (group Ib) afferents recorded during overground locomotion in normal cats. A. Top: muscle length, second panel: electromyogram (EMG), third panel: ensemble Ib firing rate profile with superimposed predicted rate derived from the EMG signal, B: muscle force as predicted from the firing rate, C: mean force in soleus obtained in separate experiments in another laboratory (Herzog et al. 1993). Reprinted from Prochazka, A., Prog. Brain Res, ©1999. pp. 133-142, with permission from Elsevier Science.

knee joint angle deg firing rate imp I s neural angular velocity deg t s knee joint angle deg firing rate imp I s angular velocity deg t s

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FIGURE 6.3 Firing rate profile of a slowly adapting type III cutaneous receptor located at "D" in the left panel recorded in a human subject with microneurography (letters A, B, and C refer to other afferents recorded in this subject). The afferent responded to knee joint displacement. The third trace on the right superimposes the instantaneous firing rate (bold) and the predicted rate derived from the joint angular velocity and joint angle signals in the two top traces. The bottom trace shows the raw action potentials of this unit. Reproduced with permission from Edin, B.B., J. Physiol., 531, 289, 2001.

FIGURE 6.3 Firing rate profile of a slowly adapting type III cutaneous receptor located at "D" in the left panel recorded in a human subject with microneurography (letters A, B, and C refer to other afferents recorded in this subject). The afferent responded to knee joint displacement. The third trace on the right superimposes the instantaneous firing rate (bold) and the predicted rate derived from the joint angular velocity and joint angle signals in the two top traces. The bottom trace shows the raw action potentials of this unit. Reproduced with permission from Edin, B.B., J. Physiol., 531, 289, 2001.

Edin 2001) and it has been argued that they probably contribute to the sense of position and motion of the extremities. There are massive numbers of skin receptors in the limbs. For example, it has been estimated that there are about 17,000 skin mechanoreceptors with myelinated afferent fibers on the surface of the human hand (Johansson and Vallbo 1979), compared to about 4000 muscle spindles, 2500 tendon organs, and a few hundred mid-range joint receptors in the whole arm (Voss 1971; Hulliger 1984). Type I skin receptors and hair follicle receptors are responsive to rapidly varying skin stimuli. Slowly adapting type II and III receptors respond sensitively to stretching of the skin and continue to signal maintained stretch (Horch et al. 1977). In two recent studies, it was shown that stretching of the skin overlying finger joints produced illusions of movement of the fingers, reinforcing the idea of a proprioceptive role for skin receptors (Edin and Johansson 1995; Collins and Prochazka 1996). Figure 6.3 shows the firing rate of a slowly adapting type III cutaneous receptor located at "D" in the left panel recorded in a human subject with microneurography. The afferent clearly provided information about knee joint displacement and velocity. Its firing profile was extremely well fitted with a first order transfer function similar to that used in the simpler models of group Ia transduction.

6.5.8 Overview of Proprioceptive Firing during Locomotion

Figure 6.4 summarizes the current knowledge regarding the firing rate profiles of ensembles of group Ia, Ib, and II muscle afferents during medium-speed stepping in cats. The data was quantified or estimated from numerous single-unit recordings obtained with microwire electrodes implanted in dorsal root ganglia of free-to-move cats (Prochazka et al. 1976; Loeb and Duysens 1979; Loeb 1981; Loeb 1984; Prochazka and Gorassini 1998a). If we assume a mean firing rate per receptor of about 75 impulses/s during locomotion (Figure 6.4), at any given moment the net input to the spinal cord from the 10,000 or so muscle afferents in each leg is between 0.5 and 1 million impulses/sec. Figure 6.4 also shows that the firing rates of muscle afferents are deeply modulated during stepping, and so in principle this would provide highly detailed information to the CNS for locomotor control.

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