Spinal and supraspinal effects of activity in ligament afferents
Introduction
Ideas of ligaments as sensory structures that, via afferent input to the CNS, contribute to proprioception, motor control and joint stability have been discussed for more than a century. As a consequence of a growing number of experimental and clinical evidence, both from studies on animals and on human subjects and patients, such sensory functions of ligaments have recently become widely accepted.
Recordings from joint and ligament afferents in animals have shown that there is a wide variety of response characteristics represented in the sensory output from ligaments (for reviews, see [1], [2], [3], [4], [5]). There are receptors within the ligaments that have low thresholds to mechanical stimulation, and others that are activated only when the tension of the ligament is very high. Among the low threshold nerve endings there are both slowly and rapidly adapting ones, whereas the high threshold endings appear to be mainly slowly adapting. Although there are nerve endings in the joint that are active throughout the normal range of joint rotation, it has been demonstrated that the majority of the low threshold nerve endings of the joints are most active when the joint approaches the limits of its normal working range. Nevertheless, the fact that the ligaments contain mechanosensitive nerve endings with low thresholds and with static and dynamic response qualities, clearly suggest that these nerve endings are involved in providing the CNS with information about joint positions and movement.
Afferents emanating from joint mechanoreceptors have been shown to project to spinal motoneurones and interneurones, as well as to a number of supraspinal structures. Fig. 1 shows a schematic representation of the principal pathways by which mechanosensitive ligament receptors can contribute to joint stability, muscle co-ordination and proprioception. The conscious ability to recognise positions and movements of our extremities in relation to each other and the body can be transmitted to cortical areas through direct spinal actions on ascending pathways, or indirectly through reflex effects on the γ-muscle spindle system. The latter implies that signals from ligament afferents, via reflex actions onto γ-motoneurones, are integrated in the proprioceptive input provided by the primary and secondary muscle spindle afferents. The ligament afferents can contribute to motor control and co-ordination through polysynaptic interneuronal pathways, and, again, via reflex actions on the γ-muscle spindle system.
In addition to the sensory properties, the ligaments have a mechanical role by causing restraints to hyper-rotation of the joint (Fig. 1). However, the functional stability of the joint (i.e. stability during active movements) is not only a result of the mechanical properties of the ligaments, but also of the restraint caused by the joint capsule, the joint geometry, the friction between the cartilage surfaces, and the compression force caused by the body weight and the muscle activity around the joint. Among these factors, an appropriately adjusted muscular activation pattern around the joint has been convincingly demonstrated to be of crucial importance (for references, see [5], [6], [7], [8]). Thus, since afferents originating in ligaments are involved in the control of muscle stiffness and co-ordination, it can be conclude that the ligaments contribute to the functional joint stability by a combination of their mechanical and sensory characteristics (Fig. 1).
The objective of the present review is to give a brief overview of available knowledge on effects from joint and ligament afferents on spinal and supraspinal structures, and to discuss some functional implications of these observations. Special emphasis has been put on interpreting known effects on supraspinal structures, skeletomotoneurones and the γ-muscle spindle system.
Section snippets
Ascending pathways, supraspinal projections and proprioception
Most knowledge on supraspinal projections from joint afferents originates from electrophysiological studies made on cats and monkeys. The pioneering work was made by Mountcaste and Gardner in the mid 20th century (e.g. [9], [10], [11], [12], [13], [14]). Based on their and others work it has become evident that information from joint afferents reaches supraspinal structures via several ascending pathways. Thus, signals from joint afferents are transmitted, through the dorsal column and the
Skeletomotoneurones and muscle responses
From early animals studies it is known that electrical activation of high threshold joint afferents elicits clear-cut reflex effects on skeletomotoneurones (α-motoneurones). The reflex actions induced from these afferents, which largely emanate from nociceptors, are characterised by excitatory effects on flexor motoneurones and both excitatory and inhibitory effects on extensor motoneurone [24], [25]. Joint afferents originating from low threshold mechanosensitive receptors, on the other hand,
The γ-muscle spindle system
It has been firmly established that the muscle spindle afferents have a crucial role in position and movement sensations (for reviews, see [[4], [41], [42]]). This has become evident from a number of observations, of which the most important are that:
- 1.
muscle spindle afferents have strong projections to several supraspinal structures, including cortical areas;
- 2.
activation of muscles spindle afferents, by muscle vibration in a stationary limb, induce illusions of joint movements;
- 3.
removal of input
Coding of afferent information
The research on neuronal coding of peripheral inputs has for a long time been dominated by studies aimed at identifying receptor properties and pathways that transmit specific sensory modalities or qualities. As a result, sensory endings in peripheral tissues have been divided into different modality specific categories, like e.g. touch, pressure, vibration, muscle length, muscle force, ligament tension, temperature, and chemosensitive receptors. Attempts have also been made to subdivide
Reflex regulation of muscle stiffness and joint stability
As discussed above there are several lines of arguments against a significant role of ligament afferents as initiators of joint protective reflexes through servoregulation mechanisms (see 3. Skeletomotoneurones and muscle responses). The major limitation in these feedback mechanisms is that they are slow, i.e. they involve a certain delay between the time at which a stimulus is applied and activates peripheral sensory endings, and the initiation of the motor response or movement adjustment.
Acknowledgements
The financial support from The Swedish Council for Work Life Research, Inga-Britt and Arne Lundbergs Forskningsstiftelse, and The Saami Parliament of Sweden (mål 1 Sápmi) is gratefully acknowledged.
Per Sjölander graduated in 1986 from the University of Umeå (Sweden) with a B.Sc. degree in Biology and Zoology. His postgraduate studies involved electro-physiological examination of effects on motor control and proprioception elicited by activation of nerve endings in different joint structures. For these studies he earned a Ph.D. from the University of Umeå in 1989. He continued his work as an assistant professor at the University of Umeå until 1992, when he moved to Canada to commence a
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Cited by (0)
Per Sjölander graduated in 1986 from the University of Umeå (Sweden) with a B.Sc. degree in Biology and Zoology. His postgraduate studies involved electro-physiological examination of effects on motor control and proprioception elicited by activation of nerve endings in different joint structures. For these studies he earned a Ph.D. from the University of Umeå in 1989. He continued his work as an assistant professor at the University of Umeå until 1992, when he moved to Canada to commence a 2-year post-doc training period at the Department of Clinical Sciences, University of Calgary. In Calgary he studied sensory properties of Golgi tendon organs in an animal model. In 1994 he received an associate professorship at the Swedish National Institute for Occupational Health in Umeå, where he began studying the pathophysiology behind chronic musculoskeletal pain conditions. After a year as principal at the senior high school in Storuman, Sweden (1996–97), he has held the post as director at the Southern Lapland Research Department, Vilhelmina, Sweden. Over the last few years his research interests have been expanded to include clinical studies of the efficiency of various treatment and rehabilitation methods fro chronic musculoskeletal pain conditions, and epidemiological studies of the health and living conditions of the Sami people (the natives of Scandinavia). He is a member of the International Brain Research Organization, the European Neuroscience Association, the Society for Neuroscience, and the Nordic Society for Physiology.
Mats Djupsjöbacka graduated in 1989 from the University of Umeå (Sweden) with a B.Sc. degree in biology. His postgraduate studies involved electrophysiological examination of the reflex regulation of the muscle spindle system from chemosensitive muscle afferents and joint afferents in animal models. He earned a Ph.D. from the University of Umeå in 1996. Following that he did a one-year post-doc training period at the Department of Clinical Sciences, University of Calgary. In Calgary he studied fatigue related changes in electrophysiological and mechanical properties of single motor units. After his post-doc he returned to Umeå to work as an assistant professor at the Centre for Musculoskeletal Research, National Institute for Working Life. Over the last few years his research interests have focused on the pathomechanisms behind work related musculoskeletal disorders, with an emphasis on the effects of muscle pain and fatigue on proprioception and motor control.