Muscle spindles, Golgi tendon organs, and the neural control of skeletal muscle JOHN N. HOWELL, Ph.D. Ohio University College of Osteopathic Medicine Athens, Ohio MARC D. BINDER, Ph.D. University of Washington School of Medicine Seattle, Washington anatomical grounds, it is clear that the tral connections studied.8 Available evi- T. RICHARD NICHOIS, Ph.D. spindles are arranged parallel to the ex- dence indicates that activation of the Ib Emory University trafusal muscle fibers and are thus suited sensory fibers, like the activation of cuta- Atlanta, Georgia to sensing length changes of the muscle. neous aiTerents, can cause either excit- GERALD E. LOEB, M.D. The tendon organs, on the other hand, are atory or inhibitory postsynaptic poten- National Institutes of Health tials to occur in motoneurons.s The site of Bethe&, Maryland located in series with the muscle fibers and are thus suited to detecting force gen- integration involving the Ib input as well erated by the muscle fibers. Spindles have as inputs from other areas within the cen- been known for some time to be sensitive tral nervous system appears not to be the The purpose ofthis report is to share with to very small perturbetions in muscle motoneurons, but rather interneurons in the readershia of JAOA. hiahliahts of a length, producing a reflex activation, or laminae V and VI. symposium hdd at the 30tc ~nnualRe- shortening, of the muscle being Dr. Nichols traced the development of search Conference of the AOA in March stretched. In contrast, tendon organs theories concerning the mechanical as- 1986. The invited speakers in the sym- were thought to respond only to high lev- pects of the spindle-mediated stretch re- posium were Dr.-Gerald E. Loeb of the els of force and to provide protection flex and went on to point out that most of National Institutes of Health, who also again& the development of too much force our knowledge has been based on the delivered the keynote address, Dr. Man: by inhibiting the homonymous muscle ~tudyof single muscles. He stressed the D. Binder of the University of Wash- (i.e., muscle of origin of the reflex). need for extending the analysis of stretch ington, and Dr. T. Richard Nichols of Recent work has shown this idea about reflexes to groups of synergistic muscles Emory University. Dr. John N. Howell of tendon organ function to be unlikely.3.4 acting together upon a joint. A rather ex- the Ohio University College of Os- Each tendon organ provides a point of treme view of the role of the stretch reflex teopathic Medicine, program chairman insertion for 3 to 25 muscle fibers.6 Ex- system was proposed in 1953 by Mertonlo for the 1986 conference, acted as moder- perimental stimulation of a single motor who hypothesized that normal activation ator for the symposium. unit, one or more fibers of which insert on of muscle might always be preceded by In introducing the symposium, Dr. a given tendon organ, will stimulate that gamma activation of the muscle spindles, Howell pointed out that the traditional organ, producing a train of spikes in Ib and the resultant stimulation of Ia af- importance of somatic dysfunction and its afferent neurons to the spinal cord. Stim- ferent~would in turn provide the excit- treatment in osteopathic practice has led ulation of a motor unit which hasno fibers atory input to the alpha motor neurons to a natural interest within osteopathic inserting on a particular tendon organ and cause muscle contraction. This the- medicine in the aroblem of control of skel- mmetimes silences that tendon or'gan if it ory was referred to as the "follow-up etal muscle fun'ction. In 1974, Korr pub- has been previously activated by sus- length servo hypothesis." It stressed the lished an important article entitled, tained stretch of the muscle. This pre- feedback control of muscle length and the "Roprioceptors and somatic dysfunc- sumably results from unloading of the primacy of gamma activation for muscle tion."l In it he related the clinical find- tendon organ by virtue of contraction of contraction. It is now known, however, for ings of osteopathic practitioners to what adjacent muscle fibers. Each tendon many movements, including ballistic was then knowh about the physiology of organ appears to provide insertion for fi- types and patterned activities of a re- the proprioceptive organs within skeletal bers from motor units producing a wide petitive nature, simultaneous activation muscle. Specifically, he postulated that range of forces. Thus, each organ may of both gamma and alpha motor neurons alterations of the gain of the stretch re sample muscle activity over the full range occurs, generally referred to as coactiva- ceptor system might contribute to the of force development, from the small tion.11 Because the larger alpha motor etiology of somatic dyefunction and to its motor units that are the first to be re- neurons conduct action potentials faster treatment through osteopathic manip- cruited to the large units that are re- than the smaller gamma fibers, coactiva- ulative treatment. Korr's hypothesis has cruited only during maximal con- tion implies that extrafusal muscle fibers been widely accepted within osteopathic tractions. This means that the tendon must be activated before intrafusal fibers. medicine because it provided a mecha- organ input to the cord is not restricted to Thus the initial phase of contraction oc- nism that appeared to be consistent with conditions of high force development but curs independently of any feedback con- a good deal of clinical experience. can be graded over the entire range of tribution from the muscle spindle system. However, as Korr pointed out in a recent muscle force. F'urthermore, it was pointed out that the article,2 his h*thesis still awaits test- Determination of the effect of Golgi ten- Golgi tendon organs might also play an ing in the laboratory. Since the publica- don activity on neurons within the spinal important role in feedback control, so tion of Ko~r'shypothesis, additional cord has been difficult because it has not that not only muscle length, but some information has come to light about the been possible to selectively stimulate the function of both force and length would be function of muscle proprioceptors. The tendon organs or their Ib afferent fibers controlled.l2 goal of the symposium was to summarize without at the same time stimulating the The latter idea was extended further by this newer information so that it might be muscle spindles or their Ia sensory fibrs. Houk>3 who suggested that the param- available for integration into thinking Recently it has been shown that applica- eter controlled bv stretch reflex might be about the pathophysiology and treatment tion of prolonged, high-frequency, low- stiffness, definid as the ratio of force of somatic dysfunction. amplitude vibration to muscles, which is , change to length change. Nichols and Dr. Binder led off wi* a summary of an effective stimulus to the muscle spin- Houkl4 demonstrated that the linearity the traditional ideas about how muscle dles: can cause a transient elevation of , of the spring-like behavior of muscles in epindles and Golgi tendon organs func- the electrical thresholds of the Ia fibers.7 the decerebrate cat preparation was lost tion and then focused on newer informa- Under these conditions the Ib fibers can when the proprioceptive feedback loop tion about the tendon organs. On be eelectively stimulated and their cen- was i~terrupted,i.e. when the dorsal continued on page 6001117 Sept. 1986lJournalof AOAIvol. 86lno. 9 roots were cut. In the absence of reflex spinal cord from the muscle spindles in may become uncoupled so that each zone control, muscles demonstrated highly behaving animals correlate with length generates signals independently,produc- nonlinear properties which included a or velocity or any other identifiable vari- ing irregular interspike intervals and a I brief failure, or yield, of force generation able. noisy signal. Thus, the job of the gamma when the active muscle was stretched. Dr. Loeb described experiments carried program appears to keep the spindle ad- The linearization and maintenance of out in his laboratom at NIH on conscious justed so that the firing rate in the sen- the spring-like properties of muscle and animals carrying surgically implanted sory Ia fibers is kept within the appropri- the enhancement of stiffness by the muscle length and force transducers, ate range for optimal signaling. This / stretch receptors occurs in both the exten- EMG electrodes, electrodes for recording appears to occur in the cat during pre- mrs and flexore ofthe feline ankle, but not Ia units from a lumbar dorsal root gang- programmed motor patterns such as loco- equally so. Reflex action is weaker in the lion, an electrode CUEaround the femoral motion and even paw-shaking, but does flexors than in the anti-gravity extensors. nerve for recording nerve activity and for not occur in response to single unexpected However, this inequality ie not intrinsic irrigation of the nerve ~lthlocal anes- perturbations.1S to the musclea; it is a function of the or- thetic from an external syringe, and elec- The question remains as to just what is ganization of the neural control system. trodes for stimulating the saphenous being sensed and regulated by the spindle Certain brain stem lesions can alter rela- nerve and the nerve to the ham- system. The possibilities provided by the tive reflex strength, and it has now been strings.1618 The results showed that no gamma system suggest that different pa- &own that monosynaptic reflex strength simple correlation between Ia Aring and rameters can be regulated depending on can be changed through operant con- length or velocity exists.