Sensorimotor disturbances in neck disorders affecting postural stability, head and eye movement control

The amount of intramuscular connective tissue (IMCT) and its morphological distribution is highly variable between muscles of differing function. The functional roles of this component of muscle have been poorly understood, but a picture is gradually emerging of the central role this component has in growth, transmission of mechanical signals to muscle cells and co-ordination of forces between fibres within a muscle. The aim of this review is to highlight recent advances that begin to show the functional significance of some of the variability in IMCT. IMCT has a number of clearly defined roles. It patterns muscle development and innervation, and mechanically integrates the tissue. In developing muscles, proliferation and growth of muscle cells is stimulated and guided by cell-matrix interactions. Recent work has shown that the topography of collagen fibres is an important signal. The timing and rates of expression of connective tissue proteins also show differences between muscles. Discussion of mechanical roles for IMCT has traditionally been limited to the passive elastic response of muscle. However, it is now clear that IMCT provides a matrix to integrate the contractile function of the whole tissue. Mechanical forces are co-ordinated and passed between adjacent muscle cells via cell-matrix interactions and the endomysial connective tissue that links the cells together. An emerging concept is that division of a muscle into fascicles by the perimysial connective tissue is related to the need to accommodate shear strains as muscles change shape during contraction and extension.

The structure and functional significance of variations in the connective tissue within muscle.

Study design Cadaveric dissections were used to study muscle morphometry. Objective To describe systematically the musculotendinous lengths, fascicle lengths, pennation angles, and physiologic cross-sectional areas of neck and shoulder muscles implicated in head movement. Summary of background data In previous studies of neck-muscle anatomy, researchers described only a subset of muscle features, often using crude or indirect methods. None used microdissected muscles to correct measured parameters for the presence of multiple fiber compartments, internal aponeuroses, or variations in fiber or sarcomere length required for qualitative models of force-generating capabilities. Methods Muscle mass, pennation angle, fascicle length, and sarcomere length were measured in 14 neck muscles from 10 human cadavers. Architecturally complex muscles with multiple attachments were divided into subvolumes, and each subvolume was examined from both the superficial and deep surfaces, Internal aponeuroses were microdissected within muscles to characterize architectural specializations. Physiologic cross-sectional areas were calculated from the morphometric data. Results The neck musculature was architecturally complex. Many muscles crossed two or more joints and had multiple attachments to different bones. In some, the presence of tendons and aponeuroses was associated with specializations in fascicle organization. Considerable interindividual variation was found in the number and location of tendinous insertions of the scalenes and longissimus capitis muscles. In addition, rhomboideus showed significant variations in its size and shape. The cross-sectional areas of neck muscles from large and small subjects did not scale proportionately with body height and weight, nor did individual muscles with widely varying cross-sectional areas (0.3-15.3cm2) scale from on subject to another. Conclusions The accuracy of morphometry can be improved by incorporating measurements made by microdissecting neck muscles. The presence of aponeurotic attachments can greatly shorten fascicle length; failure to identify such attachments can lead to underestimates of cross-sectional areas. Accuracy of a generalized model of the neck is also improved by normalizing sarcomere lengths in all muscles.

Morphometry of human neck muscles.

This review article is designed to expose physical therapists to an examination of muscle organization and the implications that this organization has for therapeutic applications. The partitioning hypothesis is based on the fact that an individual muscle is arranged in a more complex array than simply fibers attaching at aponeuroses, tendons, or bones with a single muscle nerve innervation. Neuromuscular compartments, which are distinct subvolumes of a muscle, each innervated by an individual muscle nerve branch and each containing motor unit territories with a unique array of physiological attributes, are described. In addition, the organization of individual muscles into these subunits is paralleled by the organization of their parent motoneurons within the spinal cord. These notions are detailed in a review of data derived from studies performed primarily in cat and rat models. Recent data derived from morphological and anatomical study of human muscles support the existence of similar neuromuscular partitions. These data are complemented by physiological studies, the results from which suggest that partitions may have functional or task-oriented roles; that is, different portions of one muscle may be called into play depending on the task demands of the situation. The importance of these observations for reconsidering how we provide clinical applications, such as neuromuscular stimulation or kinesiological monitoring, is discussed.

Compartmentalization of Muscles and Their Motor Nuclei: The Partitioning Hypothesis

Intramuscular connective tissues are continuous to extramuscular connective tissues. If force is transmitted there, differences should be present between force at proximal and distal attachments of muscles. Extensor digitorum longus (EDL), tibialis anterior (TA), and extensor hallucis longus muscles (EHL) were excited simultaneously and maximally. Only EDL length was changed, exclusively by moving the position of its proximal tendon. Distal force exerted by TA + EHL complex was not affected significantly. Proximal and distal EDL isometric force were not equal for most EDL lengths: Fprox – Fdist ranged from 0 to ≈+22.7% of Fprox at higher lengths and from 0 to ≈–24.5% at the lowest lengths. It is concluded that extramuscular connections transmit force from muscle. Significant proximo-distal differences of EDL force remained after repeated measurements, regardless of length order, although their length dependence was altered. Measurements of both proximal and distal EDL force were highly reproducible, if EDL did not attain higher lengths than target length. After being active at high lengths, proximal and distal length–force curves were altered at low lengths but not for the highest length range. Extensor digitorum longus length–active force hysteresis was present for proximal as well as distal EDL measurements with increasing and decreasing isometric length order. Further isolating EDL removed the proximo-distal difference for active EDL force. However a decreased difference for passive EDL force remained, which was ascribed to remaining extramuscular connective tissue linkages. It is concluded that extramuscular myofascial force transmission is an important feature of muscle that is not isolated from its surrounding tissues.

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Extramuscular myofascial force transmission within the rat anterior tibial compartment: proximo-distal differences in muscle force.

The morphometry, histochemistry, and biomechanical relationships of rectus capitis muscles were examined in adult cats. This family of muscles contained six members on the dorsal, ventral, and lateral aspects of the upper cervical vertebral column. Three dorsal muscles (rectus capitis posterior major, medius, and minor) formed a layered complex spanning from C1 and C2 to the skull. Rectus capitis posterior major was composed predominantly of fast fibers, but the other two deeper muscles contained progressively higher proportions of slow fibers. One ventral muscle, rectus capitis anterior major, was architecturally complex. It originated from several cervical vertebrae and appeared to be divided into two different heads. In contrast, rectus capitis anterior minor and rectus capitis lateralis were short, parallel-fibered muscles spanning between the skull and C1. The ventral muscles all had nonuniform distributions of muscle-fiber types in which fast fibers predominated. Dorsal and ventral muscle groupings usually had cross-sectional areas of 0.5 cm2 or more, reflecting a potential capacity to generate maximal tetanic force in excess of 9 N. Biomechanical analyses suggested that one muscle, rectus capitis lateralis, had its largest moment in lateral flexion, whereas the other muscles had large, posturally dependent moment arms appropriate for actions in flexion-extension. The observation that most rectus muscles have relatively large cross-sectional areas and high fast-fiber proportions suggests that the muscles may have important phasic as well as postural roles during head movement.

Suboccipital muscles in the cat neck: morphometry and histochemistry of the rectus capitis muscle complex.

The feline anterior sartorius is a long strap-like muscle com- posed of short muscle fibers. Nerve branches that enter this muscle contain the axons of motor units whose constituent muscle fibers are distributed asymmet- rically within the muscle. In the present study, twitch and tetanic isometric contractions were evoked by stimulating individual nerve branches while muscle force was recorded and intramuscular length changes were monitored optically by the movement of reflective markers on the muscle. Contractions elicited by stimulating the parent nerve produced little change in the positions of the surface markers. Contractions elicited by stimulating the proximally or distally directed nerve branches caused the muscle to shorten at the end closest to the nerve branch and lengthen at the opposite end. Some muscles were supplied by a centrally directed nerve branch whose stimulation produced variable effects: in some cases a portion of the muscle shortened whereas the rest lengthened, but in other cases, the positions of the surface markers showed little change. The intramuscular length changes produced by stimulating single nerve branches were greater during isometric contractions at short whole-muscle lengths than at long whole-muscle lengths. The twitch and tetanic length-tension relationships obtained by stimulating the individual nerve branches were not congruent with the length-tension relationship pro- duced when the parent nerve was stimulated. At short whole-muscle lengths, stimulation of a single nerve branch generated only a small fraction of the force that could be generated by the muscle when the parent nerve was stimulated. As whole-muscle length increased, an increased fraction of total muscle force could be generated by stimulating a single nerve branch. The results suggest that a complex relationship between passive and active elements contributes to the total muscle force and depends on the distribution of active and passive muscle units throughout the muscle. o 1992 Wiley-Liss, Inc.

Neuromuscular organization of feline anterior sartorius: II. Intramuscular length changes and complex length-tension relationships during stimulation of individual nerve branches.

The neuromuscular organization of feline anterior sartorius was examined using three experimental approaches. First, the branching pattern of the nerve supplying anterior sartorius was inspected in muscles taken from a large number of feline cadavers. All muscles were found to be supplied by two major nerve branches, one directed proximally and the other directed distally, and most muscles (42/51) had a third distinct branch that entered the muscle centrally. Second, the motoneuronal populations supplying the three nerve branches were investigated by electrophysiological techniques. Motoneurons that supplied axons to the distally-directed branch did not appear to have collaterals in more proximally-located branches. In contrast, other motoneurons supplying the proximally-directed branch also appeared to supply axon collaterals to the centrally-directed branch. This result suggested that the motoneuronal population of the distally-directed branch was largely separate from that supplying the proximally- and centrally-directed branches. Third, the motor unit territories supplied by different nerve branches were mapped using glycogen-depletion methods. Muscle fibers supplied by the distally-directed nerve branch were mostly distributed to the medial portion of anterior sartorius, whereas the fibers supplied by the other two branches were generally found more anteriorly. Further, the muscle fibers supplied by an individual nerve branch were present in greater numbers at the end of the muscle closest to the entry point of that branch. Thus, the motor units supplied by discrete nerve branches were found to be distributed asymmetrically within anterior sartorius, but were arranged neither strictly in-parallel nor strictly in-series.

Neuromuscular organization of feline anterior sartorius: I. Asymmetric distribution of motor units.

Morphometric and histochemical methods were used to estimate the force-developing capabilities and fiber-type contents of four muscle complexes (rhomboideus, levator scapulae, trapezius, and sternomastoideus) that link the shoulder girdle to the skull and cervical vertebrae. Each complex contained at least two member muscles that were distinctive architecturally and often had specialized innervation patterns. Trapezius and sternocleidomastoideus were innervated by both cranial nerve XI and cervical spinal nerves. Glycogen depletion of trapezius suggested that the nerves derived from cervical roots might be entirely sensory. Muscles within each complex varied in physiological cross-sectional area from less than 0.1 cm2 to greater than 1 cm2. They showed differences in fiber-type composition that suggested specialized roles for different behaviors. The morphometric features of the cervical shoulder muscles suggest that they have considerable potential to produce head movements and should be incorporated into feline head-movement models.

D. B. Thomson

Papers

Suboccipital muscles in the cat neck: morphometry and histochemistry of the rectus capitis muscle complex.

Neuromuscular organization of feline anterior sartorius: II. Intramuscular length changes and complex length-tension relationships during stimulation of individual nerve branches.

Neuromuscular organization of feline anterior sartorius: I. Asymmetric distribution of motor units.

Morphometry, histochemistry, and innervation of cervical shoulder muscles in the cat.