the muscles and joints of the neck: their specialisation and role in head movement

Progress in Neurobiology Vol. 37, pp. 165 to 178, 1991 0301-0082/91/$0.00 + 0.50 Printed in Great Britain. All rights reserved © 1991 Pergamon Press plc

THE MUSCLES A N D JOINTS OF THE NECK: THEIR SPECIALISATION A N D ROLE IN HEAD MOVEMENT

M. B. DUTIA Department of Physiology, Medical School, Teviot Place, Edinburgh EH8 9AG, U.K.

(Received 6 November 1990)

CONTENTS

1. Introduction 1.1. Head and eye stabilising reflexes

2. The cervical vertebral column 2.1. Analysis of head-neck movement 2.2. Movements of the head and neck 2.3. Functional implications of changes in head-neck posture

3. The muscles of the neck 3.1. Structural specialisation in neck muscles 3.2. Functional implications of compartmentalisation

3.2.1. In-parallel compartmentalisation 3.2.2. In-series compartmentalisation

4. Proprioceptive sensory innervation of the neck 4.1. Sensory innervation of the cervical vertebral joints 4.2. Sensory innervation of the muscles of the neck

4.2.1. Structure and properties of tandem muscle spindles 4.2.2. Central control of neck muscle spindle sensitivity

5. Conclusions References

165 165 166 167 167 168 168 169 169 170 171 172 172 173 173 175 175 175

1. INTRODUCTION

The stabilisation of head posture, and the control of head movement, are of fundamental importance in an animal's repertoire of movements. In many animals including man, the cervical and upper thoracic vertebral joints are among the most flexible articulations of the spinal column. They allow the free movement of the head on the body, which in concert with the movement of the eyes forms the basis of much orienting, exploratory and reflex behaviour. However, the versatile mobility of the head-neck system places complex demands on the areas of the central nervous system concerned with postural stability and motor control. The mechanical characteristics of the head- neck skeletomotor system are complex, and vary in relation to the direction and velocity of head movement (Viviani and Berthoz, 1975; Winters, 1988). The head is normally held pitched slightly forward, and maintained in this position by tonic activity in the muscles of the neck (Richmond et al., 1985a; Roucoux et al., 1985; Loeb et al., 1988). It may rotate in almost any direction in three-dimensional space, with appropriate bending or rotation of the neck. Movements of the head may occur either as a result of voluntary activity by the animal or as a consequence of external forces acting upon it; they may occur relative to a stationary trunk or with a simultaneous body movement in a different direction, with greater or lesser rotation of the neck.

In a behaving animal, the neural control systems concerned with head position are required to perform two distinct but related tasks: first to stabilise the head in three-dimensional space, and secondly to execute intentional orienting movements, for example to capture a novel visual stimulus by means of a coordinated movement of the eyes and the head (for recent reviews see Schor et al., 1988; Guitton, 1988).

1.1. HEAD AND EYE STABILISING REFLEXES

In recent years the peripheral and central mechanisms concerned with stabilisation of the head and eyes have been extensively studied. Three interacting reflex systems detect and counteract unwanted displacements of the head in space: vestibulo-collic reflexes (VCR) , evoked by vestibular stimuli related to the movement of the head in space; optokinetic reflexes (OKR) , evoked by movements of the visual field in relation to the animal; and cervico-collic reflexes (CCR), evoked by changes in length of the neck muscles caused by the movement of the head relative to the body. The function of each of these reflex systems is to generate appropriate, coordinated patterns of neck muscle activity in response to head movement, so as to resist unintentional displacements of the head. Thus stimulation of the vertical semi-circular canals, for example by a nose-down movement of the head, evokes a bi- lateral reflex contraction of the dorsal neck extensor muscles that pulls the head back up into its normal

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position (the VCR; Berthoz and Anderson, 1971; Ezure and Sasaki, 1978; Ezure et al., 1978; Schor and Miller, 1981; Bilotto et al., 1982; Dutia and Hunter, 1985; Baker et al., 1985). The optokinetic system is stimulated by the movement of the visual field over the retina, and also activates the neck muscles (the OKR; Schweigart and Hoffmann, 1988). Finally, stretching of the dorsal neck muscles by the downward movement of the head also causes them to contract by eliciting cervico-collic stretch reflexes in them (the CCR; Peterson et al., 1985; Dutia and Hunter, 1985; Dutia and Price, 1987: Peterson, 1988; Dutia, 1989).

In parallel with the head-stabilising reflexes vestibular, optokinetic and cervical proprioceptive stimulation also elicits compensatory reflexes that stabilise the eyes in the head (Wilson and Melvill Jones, 1979; Waespe and Henn, t987; Baker et al., 1988). Thus, displacement of the head causes the reflex movement of the eyes in the orbits by an equal but opposite amount, through the vestibulo-ocular reflex (VOR) , optokinetic reflexes acting on extraocular muscles (OKR) , and cervico-oeular reflexes ( C O R ) elicited by stretching of the neck muscles. When activated independently under controlled experimental conditions, the optokinetic reflexes generate adequate compensatory movements of the head and eyes at low frequencies of stimulation, while at higher frequencies the vestibular reflexes (VCR and VOR) are more effective (Schor et al., 1988; Baker et al., 1988). The COR is relatively weak, while the actions of the CCR are usually limited to the muscles being stretched (Dutia and Hunter, 1985: Dutia and Price, 1987; Peterson, 1988).

With natural head movements the head- and eye- stabilising reflex systems interact synergistically to control the activity of the neck and extraocular

muscles, over the range of frequencies of perturbations normally encountered by the animal. The coordinated stability of the eyes and the head ensures a stable direction of gaze. Several authoritative reviews on the control of eye and head movement have appeared recently (head stabilisation, Schor et al., 1988; Peterson et al., 1989; head-eye coordination and the control of gaze, Waespe and Henn, 1987; Guitton, 1988; Collewijn, 1989). This article is concerned specifically with the skeleto-muscular system of the neck, and its role in head stabilisation and movement.

2. THE CERVICAL VERTEBRAL COLUMN

Movements of the head on the neck are achieved by the coordinated realignment of the cervical and thoracic vertebrae, and involve simultaneous movements around many vertebral joints. The cervical spine of most mammals consists of seven serially- articulating vertebrae (Fig. 1), while in birds this number ranges from 13 to 25 in long-necked animals such as the swan (King and McLelland, 1984). Each vertebral articulation is capable of axial rotation (along its longitudinal axis), extension or flexion (in the sagittal plane), and to some extent lateral bending (in the frontal plane). Overall, the cumulative flexibility of the cervical and thoracic joints permits large movements of the head relative to the body: in the guinea-pig, the passive neck may extend and flex through an angle as large as 1 l0 °, bend laterally by some 20 ° and rotate axially through approximately 50 ° (Vidal et al., 1988).

Movement about particular cervical joints is however more restricted than others, and imposes a degree of mechanical specialisation on the overall mobility of the cervical vertebral column (for a review see

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FIG. 1. (Top) Diagrammatic representation of the cervical vertebral column of the cat. (Bottom) Mobility of the passive human head-neck system in three planes. The histograms indicate the range of motion in flexion-extension, axial rotation, and lateral bending directions of the first three cervical joints (Skull-C 1,

C1~2, C2-C3) and the lower cervical joints (C4-C7). Data from Jofe et al. (1983).

THE MUSCLES AND JOINTS OF THE NECK 167

Richmond and Vidal, 1988). The articulation between the skull and the first cervical vertebra (the atlanto- occipital joint) allows a large amount of extension and flexion, but little or no axial rotation (Fig. 1; Jofe et al., 1983; Vidal et al., 1988; Richmond and Vidal, 1988). The CI -C2 (atlanto-axial)joint on the other hand is free to rotate axially through a large angle (approximately 50 ° in man, Jofe et al., 1983), but allows relatively little extension and flexion. The remaining cervical vertebrae (C3-C7) are less specialised than the atlas and axis, and have some freedom of movement in each direction. The lateral flexibility (sideways bending) of the neck is limited by the geometry of the vertebral joints and ligaments, and involves mainly the lower cervical and upper thoracic vertebrae (Fig. 1; Winters, 1988; Richmond and Vidal, 1988).

Thus anatomical specialisation of the neck vertebral column imposes mechanical restraints on the freedom of movement of the head-neck system in different planes. Movements of the head on the neck are not accommodated evenly over the serial linkages of the entire cervical vertebral column, but are accommodated instead by movements around particular vertebral joints or groups of joints, depending on the direction and amplitude of head displacement. Further specialisation of neck vertebral motion occurs as a consequence of the posture that the head-neck system adopts in the awake animal (Section 2.2).

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2 .1 . ANALYSIS OF HEAD--NECK MOVEMENT

A particular final position of the head may be achieved by different amounts of movement at a number of cervical and thoracic joints, within the mechanical restrictions inherent in the structure of the cervical vertebral column. In order to determine how movements of the head on the neck are coordinated it is necessary to understand the dynamics of cervical vertebral column motion and its control by neck muscles during head movements.

Head position or movement is commonly described in terms of nose-up or nose-down pitch, ear-up or ear-down roll, or left or right yaw (e.g. Baker et al., 1985; Richmond and Vidal, 1988). These terms are used in relation to a "normal" position of the head, that is the characteristic head posture adopted by the awake animal at rest. Typically this posture brings the horizontal semicircular canals and the utricular maculae of the two sides within a few degrees of the earth-horizontal plane (Girard, 1930; de Beer, 1947; Curthoys et al., 1975; Wilson and Melvill Jones, 1979; Vidal et al., 1988). It is thus implied that the normal position of the head is maintained in a vestibular- receptor oriented reference frame.

However, these terms define only the position of the head in space, and are independent of the orientation of the cervical spine. An animal lying on its side, for example, may raise its head into a "normal" upright position by the appropriate elevation and rotation of the cervical vertebral column. In this new posture the remaining freedom of movement of the neck vertebral joints, the length-tension characteristics of the muscles of the neck, and the patterns of neuromuscular activity required to control the head- neck system are clearly different from when the body is also upright.

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FIG. 2. A coordinate system for the description of the orientation of the cervical vertebral column in terms of the relative positions of the individual vertebrae. The angles A and B represent the angular displacement of a vertebra relative to its neighbour, in one plane. The absolute orientation of the vertebral column in space may be obtained with reference to, for example, the earth-horizontal plane.

(After Vidal et al., 1988.)

For a complete description of the orientation of the head-neck system, it is therefore necessary to define not only the orientation of the head in space but also its position relative to the cervical vertebrae and, consequently, the rest of the body. Towards this end, Panjabi et al. (1974) proposed an orthogonal coordinate system to describe the orientation of each vertebra relative to its neighbours (Fig. 2). This method has been employed by Vidal et al. (1986, 1988) to analyse head and neck movements in animals using fluroscopic imaging to visualise the neck vertebrae (see below). However, the accuracy of this technique depends on precise information about the three- dimensional position of each of the neck vertebrae, which may be too difficult to obtain in many experimental situations. A number of other techniques, using for example electromagnetic search coils (Collewijn, 1979), fluid-filled length gauges such as those devel- oped for the recording of movements of the limbs (e.g. Prochazka, 1984), or electrogoniometric devices (Alund and Larsson, 1990) may be useful for recording the overall position of the head relative to the body, but these would not provide detailed information about the position or movement of individual neck vertebrae.

2.2. MOVEMENTS OF THE HEAD AND N E C K

Head movements may be made either in a distributed manner with small movements of many serially- linked vertebrae, or in a more concentrated manner around a small number of appropriate joints while the remainder are actively stabilised by compensatory neck muscle activity (Richmond and Vidal, 1988).

168 M. B. DUTIA

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FIG. 3. Diagrammatic representation of the "resting posture" of the head-neck system in an alert animal at rest. Note the near-vertical orientation of the major part of the cervical vertebral column (C2-C5). The rostral joints (Skull-C 1, C lqE2) are held in flexion, bringing the skull into its normal near-horizontal orientation. The cervico-thoracic joints (C5-Th2) are held nearly-fully extended. (After Vidal

et al., 1986, 1988; Richmond and Vidal, 1988.)

There is evidence that head-neck movements are concentrated around particular vertebral joints, from the studies of Vidal e t al. (1986, 1988) and Richmond e t al. (1988) using fluroscopic video-imaging to visualise the neck vertebral column. In an awake animal at rest, the major part of the cervical spine (C2~C5) is held in a characteristic near-vertical posture that is similar in several species ranging from the guinea-pig to man (Fig. 3). This resting posture is attained by holding the lower cervical vertebral joints (C5-C7) nearly fully-extended (Fig. 3, lower arrow), and the upper joints (Skull--C1, CI-C2) nearly fully-flexed (Fig. 3, upper arrow). Presumably this neck posture is the most energy-efficient for the support of the weight of the skull against gravity, reducing to a minimum the degree of tonic neck muscle activity required (Loeb et al. , 1988). The curved cervico- thoracic region of the spine with its associated muscles and ligaments may also act as a damping or shock-absorbing system that isolates the head from perturbations affecting the body (Vidal et al. , 1986, 1988).

This characteristic resting posture of the cervical spine imposes further, "neuromuscular" restrictions on the freedom of movement of the neck vertebral joints. Since the upper cervical joints (Skull-C1, C1-C2) are held nearly fully flexed at rest, they can participate only to a limited extent in downward movements of the head (Fig. 3). Similarly the lower cervical joints may contribute little to upward movements of the head, as in the resting posture they are nearly at full extension. Thus head movements in the sagittal plane may be expected to occur in a concentrated manner around the skull/C1/C2 joints and the cervico-thoracic region of the neck (Vidal e t al. , 1986, 1988).

Movements of the head in other planes also probably occur in a concentrated manner around particular vertebral joints. In man, horizontal turning movements of the head occur primarily around the C1-C2 joint, with the remainder of the cervical spine involved only in large head turns (Winters, 1988). Lateral bending largely involves the lower cervical and thoracic vertebrae, particularly in quadrupeds (Fig. 1; Richmond and Vidal, 1988).

The mechanical and neuromuscular factors that determine the motion of the neck vertebral joints during various head movements are still to be fully elaborated. An understanding of the dynamics of neck motion is likely to be important not only in revealing the neuromuscular mechanisms that bring about coordinated movements of the head, but also in assessing the significance of neck proprioceptive afferent feedback from particular joints in the control of head movements that involve those joints.

2.3. FUNCTIONAL IMPLICATIONS OF CHANGES IN HEAIY-NECK POSTURE

The resting posture documented in the above studies is probably one of several preferred orientations that the head-neck system may assume under different circumstances. For example, it is abandoned when the animal begins to locomote (Vidal et al. , 1986). With changes in the initial posture of the head-neck system the function of the upper and lower cervical spinal column may change significantly. When the head is lowered for example, the cervico-thoracic joints presumably flex and come closer to their mid-range position, while the upper cervical joints remain more or less as flexed as before. The lower cervical spine may then participate rather more significantly in head elevation than before: in effect, the patterns of neuromuscular activity required for head elevation may depend significantly on the starting head-neck orientation. It is also likely that the mechanical filtering characteristics of the cervical vertebral column will vary dynamically with changes in the head-neck posture, depending on the articular mobilities and the length-tension relations of their associated muscles. Thus perturbations of head- or body-position due to external forces may have quite different effects on particular neck joints and their associated musculature depending on the initial head-neck orientation. The importance of such considerations has yet to be assessed.

3. THE MUSCLES OF THE NECK

The cervical spine is invested with a rich assembly of muscles, reflecting the versatile mobility of its joints. Some 16 or so pairs of muscles directly link the skull either to the cervical and thoracic vertebrae or to the shoulder girdle (for a detailed survey see Richmond and Vidal, 1988). These include the large muscles of the neck that act across three or more neck joints (splenius, longissimus capitis, biventer cervicis and complexus, extensors; obliquus capitis inferior and superior, flexors), as well as short sub-occipital muscles that act specifically about the upper cervical joints (the rectus capitis posterior and rectus capitis

Tim MUSCLES AND JOINTS OF ~ NECK 169

anterior muscles). In addition, each neck vertebra is linked to its neighbours by short intervertebral muscles that attach to the transverse and spinous processes. The coordinated activity of all of these muscles deter- mines the orientation of the cervical vertebral column, and the position of the head in relation to it. Still further muscles, investing the thoracic vertebrae, are also involved in controlling the position of the head and neck, as much of the lateral bending and flexion of the neck occurs at these levels (see above). Thus the control of head position and movement is a complex task which depends upon the coordination of motor activity in multiple muscle groups, innervated by motoneurone pools in the entire length of the cervical and upper thoracic spinal cord. This complexity is manifest not only in the control of voluntary head movements, but also in the dynamic stabilisation of the head through coordinated reflex responses to involuntary displacements.

3.1. STRUCTURAL SPECIALISATION IN NECK MUSCLES

The muscles of the neck possess a number of notable structural complexities, which have been best documented in the cat (for a recent review see Abrahams and Richmond, 1988). With the exception of the short intervertebral muscles, each of the neck muscles is innervated by branches of two to five spinal segmental nerves. While this is not unusual in that the well-studied muscles of the hind-limb also receive their innervation from several lumbo-sacral segments in an analogous manner, in the dorsal neck extensor muscles at least there is good evidence that the territory innervated by each spinal segment is clearly delineated. This is most obvious in the biventer cervicis muscle, which is made up of five distinct compartments arranged in series with each other (Fig. 4, Armstrong et al., 1988; Richmond and Armstrong, 1988). The compartments are separated by tendinous bands that cross the entire width of the muscle. The serial compartments are innervated by separate muscle nerves that derive from the dorsal rami of the spinal nerves of C2-C5, with the C3 spinal segment giving rise to two muscle nerves that innervate their own compartments (Fig. 4). Motoneurone axons in

these nerves innervate motor units whose constituent muscle fibres are restricted to the appropriate compartment, as demonstrated using the glycogen depletion technique (Armstrong et al., 1982, 1988). In other neck muscles such as splenius the segmental compartmental territories are not as clearly defined by tendinous inscriptions, but the in-series organisation of motor units innervated by each spinal segment is maintained (Richmond et al., 1985b).

A further level of motor unit segregation occurs in some neck muscles at least. In biventer cervicis, muscle fibres innervated by a particular motoneurone are arranged in a longitudinal column within the muscle rather than being distributed randomly (Armstrong et al., 1982, 1988). Each serial compartment is therefore further divided functionally into longitudinal strips. Medially-placed muscle fibres are more often of histochemical type SO, whereas more laterally-placed fibres tend to be of type FG, thus superimposing a medio-lateral longitudinal specialisation of motor units onto the compartmentalised architecture of the muscle (Richmond and Armstrong, 1988). It is not known how this spatially-specific arrangement of motor unit characteristics and innervation is brought about during development of the neck muscles, or if the specific pattern of motor-unit distribution remains in muscles re-innervated for example after nerve injury.

3.2. FUNCTIONAL IMPLICATIONS OF COMPARTMENTALISATION

Although it is striking that many of the large neck muscles have a compartmentalised structure as a common feature of their organisation, this is not unique to them. Recently, the extent to which compartmentalisation or part i t ioning of skeletal muscles is a general principle in motor organisation, and the possible functional implications of such an arrangement, have been the subject of debate (Stuart et al., 1988; Windhorst et aL, 1989). In this more general context, a "compartment" within a muscle is defined as a group of muscle fibres and muscle receptors which occupy a contiguous, reproducible region within a muscle and which is innervated by a branch of a muscle nerve (English and Letbetter, 1982a,b; Balice-Gordon and Thompson, 1988; Windhorst

FIG. 4. Structure of an in-series compartmentalised muscle, the neck extensor biventer cervicis. Line drawing showing the origin of the muscle on the processes of C7-T3 and its insertion on the lamboidal ridge of the skull. The solid lines (arrowed) indicate tendinous inscriptions that cross the entire width of the muscle and separate its five serial compartments. The innervation of the five compartments by separate muscle nerves originating in the dorsal rami of C2-C5 segmental spinal nerves is indicated diagrammatically. Note that the C3 segmental nerve innervates two compartments, C3-rostral and C3-caudal respectively.

(Adapted from Armstrong et al., 1988.)

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FIG. 5. Structure of an in-parallel compartmentalised muscle, the lateral gastrocnemius. (Top) Dorsolateral view of the lateral gastrocnemius muscle. (Bottom) Diagrammatic serial transverse sections illustrating the regions of the muscle innervated by different branches of the muscle nerve. (Adapted from English and

Letbetter, 1982a,b; Windhorst e¢ al., 1988.)

et al., 1989). Compartments defined in this way are not necessarily anatomically segregated by tendinous inscriptions or fascia, and may lie either in series or in parallel with other compartments. A variety of muscles have now been shown to be partitioned or compartmentalised using this definition, primarily on the basis of specific topographic innervation of intramuscular territories by motoneurone axons in different branches of the muscle nerve ("neuromuscular partitioning", Windhorst et al., 1989; Fig. 5). The neuromuscular compartments innervated by different branches of the muscle nerve can be readily demonstrated using the glycogen depletion method (e.g. Balice-Gordon and Thompson, 1988). Functional "partitioning" of hind-limb muscles is further sup- ported by the selective response of muscle mechanoreceptors to the contraction of single neuromuscular compartments ("sensory partitioning", Binder, 1986: Windhorst et al., 1989), and the localised distribution of muscle spindle and tendon organ afferent innervation within the spinal motoneurone pool ("central partitioning", Windhorst et al., 1989; Stuart et al.. 1988; Binder, 1986). The combination of neuromuscular, sensory and central partitioning gives rise to reflex localisation, the localisation of a reflex response to that part of a complex muscle to which a stimulus is applied (Windhorst et al., 1989). As an example, the cervico-collic stretch reflex is localised in the neck muscle splenius: stretching of the muscle by head movement elicits a reflex contraction mainly in the rostral compartments, while stretching imposed by moving the body relative to the head elicits reflex activity mainly in the caudal compartments, presumably because of the central partitioning of muscle spindle afferents within the splenius motoneurone pool (Bilotto et al., 1982; Ezure et al., 1983).

In this broader context, a number of hind-limb muscles are partitioned into two or more functional compartments, e.g. medial gastrocnemius (Letbetter, 1974), lateral gastrocnemius (English and Letbetter, 1982a,b), biceps femoris, semitendinosus (Bodine et al., 1982; English and Weeks, 1987), extensor digitorum longus (Balice-Gordon and Thompson, 1988), and others. Unlike the largely in-series compartmentalisation of neck muscles, however, the compart-

merits in most of these muscles are largely in-parallel, with the notable exception of semitendinosus (Bodine et al., 1982).

3.2.1. In-parallel eompartmentalisation

The functional implications of in-parallel compartmentalisation have been considered in detail by Stuart et al. (1988), and Windhorst et al. (1989). Essentially, it is proposed that in-parallel compartmentalisation of muscles and their motoneurone pools is a neuromuscular mechanism by which the nervous system may utilise particular sub-volumes of a structurally complex muscle in a flexible and task- dependent way. Thus, "partitioning may provide for the differential control of muscular regions that are specialised for diverse functional capabilities resulting from differences in fiber-type composition, pinnation, or site of attachment" (Windhorst et al., 1989). The rat EDL muscle, for example, is a pinnate muscle that contains two compartments (K and F ) arranged in parallel with each other, each innervated by a branch of the muscle nerve (Balice-Gordon and Thompson, 1988). It has four tendons of insertion which attach to digits 2-5 of the foot. Although electrical stimulation of either the K or F branches of the muscle nerve generates tension at each of these tendons, contraction of the K compartment generates more tension at digits two and three, while contraction of the F compartment generates more tension at digits four and five. Thus although in-parallel compartmentalisation of the EDL does not enable selective control of particular digits by sub-volumes of the muscle (at least in the rat), it is possible that differential activation of thc two compartments could regulate the force produced at the lateral or medial digits in a way that might be useful in balance or locomotion (Balice-Gordon and Thompson, 1988).

Selective activation of separate compartments of partitioned muscles has been demonstrated in the cat lateral gastrocnemius muscle during locomotion (English, 1984), and in a number of human forearm muscles during voluntary movements of the arm (see e.g. Gielen and Denier van der Gon, 1990). Thus experimental evidence suggests that in-parallel corn-


partmcntalisation may provide the nervous system with a degree of selective control over specialised subvolumes of an anatomical muscle, which are independently utilised in a flexible and task-oriented manner.

3.2.2. In-series compartmentalisation

In contrast to in-parallel compartmentalisation which may promote the independent use of sub- volumes of a complex muscle, in-series compartmentalisation as observed in the neck muscles imposes significant constraints that restrict the independent utilisation of separate compartments. Some of these have been studied in the semitendinosus muscle which contains two in-series compartments (Bodine et al., 1982; Botterman et al., 1983) and also in the neck muscles (Loeb et al., 1988).

For a muscle composed of in-series compartments to generate useful tension, all the compartments must contract together and generate similar tensions, even though the possibility of independent activation exists anatomically. This is to avoid the overstretching and possible damage to a weakly contracting compartment by the tension generated in its stronger-contracting neighbours. The dissipation of active tension in contracting and non-contracting compartments has been considered in detail theoretically by Morgan (1985) and experimentally by Bodine et al. (1982). The cross- sectional areas of different in-series compartments are similar in both semitendinosus (Bodine et al., 1982) and in biventer cervicis (Richmond and Armstrong, 1988), implying similar force-generating capabilities (Henneman and Olsen, 1965). Electromyographic recordings from the two compartments of semitendinosus show a double burst of activity during the step cycle, both compartments being recruited and released synchronously, at least at slow and moderate velocities of movement (English and Letbetter, 1981; Murphy et al., 1981). Emg recordings from neck muscles during head movements also show synchron- ous activation of linked compartments (Loeb et al., 1988). The synchronisation of motor unit discharges in serially-linked compartments presumably allows the spatio-temporal summation of twitch tensions of motor units across compartments, yielding effective tension at the two ends of the muscle.

In-series compartmentalisation therefore does not allow the flexible or independent activation of different compartments, in contrast to in-parallel compartmentalisation where specialised compartments may be used flexibly in a task-dependent manner. In relation to the neck muscles, neural mechanisms must exist that coordinate the discharge of motoneurones in several spinal segments which innervate a serially- linked muscle. These may involve intersegmental inter- neuronal circuitry, or may depend on strong common inputs either from higher centres or from muscle spindle afferent feedback (Loeb et al., 1988). Recent studies of the morphology of vestibulospinal axons innervating neck motoneurone pools have demonstrated their extensive branching within the ventral cervical spinal cord (Yoshida et al., 1988). This may represent the morphological basis for the distribution of a common descending drive to motoneurones located along the length of the cervical cord.

Direct evidence for the complex interactions between linked compartments in a neck muscle has come from recent experiments on the cat biventer cervicis, and is illustrated in Figs 6 and 7 (Price, 1990). Independent electrical stimulation of each of the C 1-C4 compartments of the biventer muscle produced approximately the same amount of tension, some 0.08 N during a single twitch and 0.4 N during tetanic stimulation at 50 Hz. These values are much lower than values of 1-2 N maximal tension estimated by Richmond and Armstrong (1988), presumably because of the dissipation of much of the active tension in the visco-elastic elements of the inactive compartments. With simultaneous stimulation of the C 1424 compartments the evoked tensions approached the estimated maximal value (Fig. 6). Figure 7 shows a recording of the discharge of a muscle spindle primary (bL b2c) afferent located in the C2 compartment. Contraction of this compartment silences the spindle afferent, while contraction of the adjacent C3 compartment strongly excites it. Similar effects were observed by Botterman et al. (1982) in scmitendinosus. Thus spindles in the individual compartments of serially-linked muscles respond not only to the length of their compartment but also, in the contracting muscle, to any differential length changes between compartments caused by unequal strengths of contraction. Although monosynaptic stretch reflexes are weak in the neck muscles (Keirstead and Rose, 1988), polysynaptic cervico- collie stretch reflexes are readily evoked (Dutia and Hunter, 1985; Dutia and Price, 1987; Peterson, 1988) and these may serve to correct any imbalances of active tension generation in serial compartments, lead- ing to effective tension generation in the muscle as a whole.

Thus, both neck and hind-limb muscles provide examples of compartmentalisation or partitioning in neuromuscular organisation (cf. Windhorst et al., 1989). However, the functional advantages of in-series compartmentalisation, in terms of force generation or other aspects such as fatiguability, are still not clear. Significant differences in the central control of these two types of partitioned muscle are to be expected, given the complex interactions that occur between compartments in serially-linked muscles.

Te~nic tension

ca(c) ~ - c 4 Expected Fro. 6. Tetanic tension generated in the cat biventer cervicis muscle on stimulation of either the C3 (rostral) compartment alone, or the C2-C4 compartments together (the C5 compartment was not available for stimulation). The tension evoked by C3(r) alone is much lower than expected from its cross-sectional area (cf. Richmond and Armstrong, 1988), presumably because of the other in-series compartments are slack. With simultaneous stimulation of Cl-C4 compartments the measured tension approaches the expected value.

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FIG. 7. Response of a biventer muscle spindle Ia afferent to direct electrical stimulation of its host compartment (A,B) and a neighbouring compartment (C,D). The spindle was located in the C3 (caudal) compartment. Single twitch (A) or tetanic (B) contraction of that compartment silenced the spindle afferent, while contraction of the C4 compartment excited it (C,D). (Adapted from Price and Dutia, 1987.)

4. PROPRIOCEPTIVE SENSORY INNERVATION OF THE NECK

The rich sensory innervation of the neck is a reflection of its role in proprioception (Taylor and McCloskey, 1988), and its importance in the elaboration of reflexes controlling the posture of the limbs and the trunk (Roberts, 1978; Wilson, 1984, 1988). Vestibular reflexes elicited by head movement and neck reflexes elicited by rotation of the cervical vertebrae interact to regulate the extensor muscle tone of the limbs (Lindsay et al., 1976; Roberts, 1978). In the forelimbs of the pre-collicular decerebrate cat (Lindsay et al., 1976), either reflex system when activated alone gives rise to appropriate but opposite reflex responses: a vestibular stimulus related to roll- tilting of the animal causes extension of the downhill limb, while a neck reflex stimulated by cervical vertebral rotation in the same direction causes flexion of that limb. During natural movements of the head on the neck, simultaneous vestibular and neck afferent stimulation results in mutual cancellation of their reflex effects, allowing the head to move freely without disturbing the posture of the limbs and trunk (Lindsay et al., 1976; Roberts, 1978). Recent recordings from cervical spinal interneurones that are likely to be involved in mediating neck reflexes have demonstrated the cancellation of vestibular and neck inputs at this level (Wilson, 1988). A similar interaction between vestibular and neck inputs occurs within the central cervical nucleus which relays neck afferent input to the cerebellar anterior lobe (Hongo et al., 1988), and

brainstem structures including the vestibular nuclei (see e.g. Wilson et al., 1990).

4.1. SENSORY INNERVATION OF THE CERVICAL VERTEBRAL JOINTS

The early work of McCouch et al. (1951) which demonstrated that neck reflexes were not abolished by deafferentation or removal of the neck muscles, led to the view that these reflexes were due to receptors located within or close to the cervical vertebral column. Wyke (1979) reported that slowly-adapting mechanoreceptors, similar to Ruffini endings found in other joints, were particularly common in the soft tissues around cervical vertebral joints. However, Richmond and Bakker (1982) in a detailed histological study of decalcified neck joints were unable to confirm this. Several lines of evidence now indicate that cervical joint receptors are unlikely to play a prominent role in mediating neck reflexes: for example, damage restricted to neck muscles or their nerves (Cohen, 1961; Abrahams and Falchetto, 1969), or injection of local anaesthetic into the neck muscles (DeJong et al., 1977), gives rise to postural disturbances presumably related to the disruption of neck reflexes. The frequency-response dynamics of the neck reflex in the forelimbs match the response characteristics of muscle spindle afferents, suggesting that these receptors are responsible (Wilson, 1984, 1988; Peterson, 1988). The extent to which the Paciniform corpuscles and free nerve endings found in the cervical joints contribute


to neck reflex effects has yet to be determined experimentally.

4.2. SENSORY INNERVATION OF THE MUSCLES OF THE NECK

The major part of the afferent innervation of the neck is concerned with sensory receptors in the intervertebral muscles and in the long muscles of the neck. These muscles contain relatively high densities of muscle spindles, Golgi tendon organs and Pacini- form corpuscles (Cooper and Daniel, 1956, 1963; Thompson, 1970; Richmond and Abrahams, 1975), with the intervertebral muscles in particular being extremely densely populated with muscle spindles (Richmond and Bakker, 1982; Bakker and Richmond, 1982).

The muscle spindles in neck muscles have long attracted the attention of histologists, not only for their abundance but also because of their often elaborate structure. Many spindles in neck muscles exist not as the classic single encapsulated receptor epitomised in typical hind-limb muscles, but occur instead as linked assemblages of receptors often in restricted regions of a muscle. These have been termed "conjunctive forms" of the classical spindle (Richmond and Abrahams, 1975), of which three types have been recognised: paired linkages, where two or more spindles lie in side-by-side or end-to-end contact but remain recognisably separate entities; parallel (compound) spindles, where several spindles which are separate in their peripheral parts fuse together to form a single capsule, within which the bundles of intrafusal fibres retain their individual sensory and motor innervation; and finally tandem (serial) spindles, where two to five spindles are linked together in series by a single long shared intrafusal muscle fibre (Cooper and Daniel, 1956, 1953; Barker and Ip, 1961; Richmond and Abrahams, 1975; Richmond et al., 1988). These structurally elaborate forms of muscle spindle are particularly common in the muscles of the neck, where for example some 35- 50% of the total number of spindles may participate in tandem serial linkages (Richmond et al., 1986, 1988). Tandem spindles in hind-limb muscles are less common, being some 10-25% of the total in some muscles (Barker and Ip, 1961; Richmond and Bakker, 1982).

In neck muscles a further level of elaboration is attained through the close grouping together of spindles, each of which may be of the conjunctive form, into "spindle complexes" (Richmond and Abrahams, 1975). Equivalent receptor aggregations are rarely seen in hindlimb muscles (Barker and Ip, 1961). Spindle complexes are particularly numerous in the small perivertebral muscles of the neck, where a single complex containing 5-12 spindles may extend from one end of the perivertebral muscle to the other, and may often be intimately associated with a tendon organ at one or both ends (Richmond and Bakker, 1982; Bakker and Richmond, 1982). In the long extensor muscles of the neck, a combination of a muscle spindle and a tendon organ lying end-to-end (a "dyad", Richmond and Bakker, 1982) is commonly found near areas of myotendinous contact, either at the ends of a muscle or near tendinous inscriptions.

4.2.1. Structure and properties o f tandem muscle spindles

Of this diverse range of proprioceptor configurations in the muscles of the neck, the tandem muscle spindle has been the most extensively studied. The serial encapsulations that make up a tandem spindle are not all the same, one being consistently larger and longer than the other (Fig. 8, Barker and Ip, 1961; Richmond and Abrahams, 1975b; Bakker and Richmond, 1981; Kucera, 1982; Banks et al., 1982; Richmond et al., 1986, 1988). The larger unit of the tandem spindle resembles the classical hind-limb spindle in that it contains the normal complement of two nuclear bag intrafusal fibres (bagl and bag2) and a bundle of chain fibres, and is therefore termed the b~b2c unit (Banks et al., 1982). The b~b2c unit is innervated at its centre by large-diameter myelinated afferent axons which form primary and secondary sensory endings on the intrafusal fibres, as in a typical hind-limb spindle (Hulliger, 1984; Boyd and Gladden, 1985; Hunt, 1990). However, the smaller unit of the tandem spindle contains only the bag2 intrafusal muscle fibre and chain fibres (a b2c unit, of which there may be several in series, Fig. 8). The afferent innervation of b2c units is simpler, with usually a single afferent axon forming sensory nerve terminals on the bag2 and chain intrafusal fibres.

b2c

,oo g.m

b~b2e

FIG. 8. Diagrammatic representation of a tandem muscle spindle in the cat. Note the larger b~ b 2 c spindle unit, which incorporates the normal complement of bagt, (b,), bag2 (b:) and chain (Ch) intrafusal muscle fibres. The smaller b2c spindle unit contains only the bag2 and chain fibres. P, primary sensory endings;

S, secondary sensory endings. (Adapted from Richmond et al., 1988.)

Ch

174 M.B. DUTIA

Much of the interest in tandem spindles has centred around the physiological properties of these b2c afferent axons and the possibility that, because they have no sensory terminals innervating a bag~ fibre, their responsiveness to muscle stretching may be significantly different from that of typical b t b~ c primary sensory endings, b2 c afferents may therefore represent a novel form of muscle stretch receptor, found in some abundance in neck and axial muscles. A large body of evidence from studies of hind-limb muscle spindles, particularly those of Boyd and his collabor- ators on the isolated visualised tenuissimus spindle (Boyd, 1977; Boyd and Gladden, 1985; Hunt, 1990), indicates that the different types of intrafusal muscle fibre are highly differentiated structurally and functionally. The bagl fibre, when made to contract by gamma fusimotor axons that innervate its polar regions (Fig. 8), strongly increases the dynamic- or velocity-sensitivity of b~b2c afferents, presumably through an activation-dependent change in its mechanical characteristics. In contrast the bag2 and chain intrafusal muscle fibres when activated by their own gamma fusimotor axons strongly elevate the discharge rate of b, b:c afferents, in the case of the bag: fibre largely without changing their length sensitivity. These two elements are under independent central control: the bag~ fibre is selectively innervated by dynamic gamma motoneurones and the bag: and chain fibres are selectively innervated by static gamma motoneurones, with little or no overlap. There is evidence that the static gamma motoneurones may themselves be of two types, innervating the bagz and chain fibres separately, adding to the flexibility with which the responsiveness of spindle afferents may be controlled by the nervous system (Boyd. 1986).

The lack of a bag~ fibre in b2c spindles implies that these receptors do not receive motor innervation from dynamic gamma motoneurones, and that the stretch sensitivity of b2c afferents is solely under the control of the static fusimotor system (Richmond and Abrahams, 1979; Price and Dutia, 1987, 1989). In contrast the stretch sensitivity of b~ b2c afferents is dependent upon the activity of both static and dynamic gamma motoneurones, and upon interactions between their effects on the intrafusal fibres. The functional implications of the selective control of b:c afferents by static gamma motoneurones are not readily apparent (for a discussion see Price and Dutia, 1989), and are unlikely to be clarified without a greater understanding of the role of the dynamic and static fusimotor systems in the control of movement (Hulliger, 1984).

Recently the response properties of identified b~c and blb~C afferents in neck as well as hind-limb muscles have been directly compared, to determine if the lack of a bag, fibre resulted in novel receptor properties of b2c afferents (Price and Dutia, 1987, 1989; Price, 1990). The afferents were identified by means of their responsiveness to muscle stretching in the presence of succinylcholine (SCh), which like acetylcholine causes the contracture of the bag, and bag: intrafusal muscle fibres while paralysing the nuclear chain fibres (Boyd, 1985). b~b2c afferents showed a characteristic marked increase in their dynamic response to ramp stretching (due to the contraction of the bag~ fibre) and a biassing of their rate of discharge (due to bag2 fibre contraction), while b:c afferents showed only the biassing effect without an increase in dynamic response (Fig. 9). The sensitivity of the two types of afferent to ramp stretching, small amplitude vibration and l Hz sinusoidal

(a) bib2C 200 [

a ~''~ tOOl o E •

0

2OO

150 • , , ".' %: ,',.. {,,,, ..

• , . . . . . . ,OO o I '

0

( b ) b=c

200 r

g ~ ,oo I ~k =E ~... J : •.:.

-.:..

200 [ [50

sc, i;~ , ~ ~ - - ~ ~;a~ 0 q __/--1

FIG. 9. Response of b~ b2c (top) and b:c (bottom) types of muscle spindle afferents to stretching in the presence of succinylcholine (SCh). The left panels show the control responses to repeated ramp stretches• When maximally activated by intra-arterial infusion of SCh at 100 #g/Kg/minute, b, b2c afferents showed an increase in the dynamic response and an elevated ("biased") discharge rate of about I00 imp/sec (top). In contrast b.,c afferents showed only the "biasing" of their discharge rate with no increase in dynamic response, presumably reflecting their lack of a bag I intrafusal muscle fibre. (Modified from Price and

Dutia, 1989; Fig. 2.)


stretching of the muscle were found to be remarkably similar, despite the lack of the bag~ fibre in b2c spindles. This suggests that, in the passive spindle, the bagl fibre is not the major determinant of their response to stretching. It argues against the proposal that an active stretch-induced contraction of the bagt fibre ("stretch-activation") is responsible for the dynamic sensitivity of spindle afferents (Poppele and Quick, 1981).

The succinylcholine technique described by Price and Dutia (1987, 1989) has recently been used by Taylor and his colleagues to identify b2c afferents in jaw muscles of the cat (Taylor and Durbaba, 1990). Preliminary indications from a study of spike-triggered averaging of field potentials generated by these after- ents in the motor nucleus of V indicate that b2c and b~b2c afferents from the same muscle have similar central projections (Taylor et al., 1990). The central projections of neck muscle afferents have been studied using anatomical techniques such as degeneration or labelling, and electrophysiologically mainly with electrical stimulation of the neck muscle nerves (for a review see Bakker and Abrahams, 1988). The system- atic application of the SCh method may help to avoid the difficulties in classifying spindle afferents that arise because of the short conduction distances in the neck (Richmond and Abrahams, 1979; Keirstead and Rose, 1988a,b; Price and Dutia, 1987, 1989).

4.2.2. Central control o f neck muscle spindle sensitivity

In a recent study Kasper et al. (1989) recorded the activity of neck perivertebral muscle afferents using floating wire microelectrodes implanted in the C2 dorsal root ganglion, and compared their responses to neck rotation before and after blocking extrafusal and intrafusal neurotransmission with gallamine. Muscle spindle afferents in the unparalysed cat responded to small amplitude (0.5-7.0 °, 0.2 Hz) neck rotations with low gain, while after paralysis this changed to a high gain, non-linear response. This was interpreted as evidence indicating a tonic, static fusimotor drive to the neck spindles in the decerebrate cat which in the unparalysed animal reduced the dynamic responsiveness of the spindle afferents. However, as pointed out by the authors, interpretation of these results is not straightforward because the location of the responding spindles was not known in relation to the neck-rotation stimulus which was applied around the C1422 joint. In the unparalysed cat, it is likely that the stimulus energy transmitted to spindles some distance away would be attenuated due to the decerebrate muscle tone in the neck muscles. Following paralysis much less of the stimulus energy would be dissipated in the flaccid muscles, resulting in a greater stretching of the perivertebral muscles and an apparent increase in gain of the spindle afferents. Further experiments, perhaps using a controlled stretch stimulus applied directly to the muscles, may avoid this difficulty.

5. CONCLUSIONS

Developments over the past 10 years in understanding the structure and function of the head-neck

skeletomotor system have emphasised its relative complexity in comparison with, for example, the better-studied hind-limb. The segmented skeletal framework of the cervico-thoracic spine enables the head to move in almost any direction in three dimen- sions, under the control of the elaborate musculature linking the head and the body. Despite its complexity the head-neck system is an attractive model for the experimental study of neural systems controlling voluntary and posturai skeletal muscles. Detailed inves- tigation of the functional organisation of the head-neck skeletomotor system may reveal more of the central and peripheral mechanisms involved in the motor control of complex body segments and their musculature.

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the muscles and joints of the neck: their specialisation and role in head movement

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