Review Article

Golgi Organs Update with Relevance to Stretching and in Dancers

Marjorie Moore, P.T., M.S.(Kines), Ph.D.

Abstract tension. 2. GTO sensations probably do o succeed, dancers have to train This article reviews the neuroscience of the reach the cerebral cortex, buried in the their bodies to high levels in a , a type of muscle sen- fissure between the motor and sensory variety of capacities. The devel- sory . The intent is also to update cortex “strips.” This information allows Topment of flexibility and other physical and correct erroneous notions regarding its dancers to know where their limbs are in capacities are dependent on neurologi- functional significance, particularly related space. GTOs also provide unconscious cal circuits and functions. Knowledge to its involvement in reflexes, propriocep- proprioception, via the , which of these concepts can be used to help tion, and stretching techniques used in helps dancers to learn new motor skills dancers and teachers approach training dance training. Historical research about and improve execution of movements. in an intelligent and effective manner. the function of the Golgi tendon organ 3. The GTO and its reflex (autogenic (GTO) has led to four erroneous views: inhibition) reduce, but do not shut off, The purpose of this article is to review 1. The GTO serves a protective function the excitability of the motor and the of the Golgi tendon organ by responding only to muscle tension its innervated muscle. The ultimate reflex (GTO), one of many types of sensory at the extreme end-range of motion; 2. effect depends on the sum of multiple receptors in muscles, , and Sensations from GTOs do not reach the other inputs on the . GTO joints. These receptors all play a role cerebral cortex and therefore serve no role input may reduce muscle activity, but does in spinal reflexes and also in our in conscious proprioception and kines- not “turn it off.” 4. During contract-relax of body movement or proprioception. thesia; 3. The GTO and its reflex circuit stretching, the GTO autogenic reflex cre- This article will update knowledge (autogenic inhibition) prevent its muscle ates inhibition that lasts only as long as about GTO function. A discussion of from contracting by “turning it off”; and the muscle’s active contraction. Therefore, its functional significance will follow, 4. During contract-relax stretching, the GTO activity is unlikely to significantly related primarily to muscle stretch- GTO autogenic inhibition reflex circuit affect the subsequent relaxation phase of is responsible for the muscle relaxation the stretch. Other receptors and spinal ing techniques used in dance and to phase and the accompanying increased circuits likely serve this function. It is proprioception. An understanding of range of motion. hoped that this updated information GTO function will enable dance ki- Recent research has shown that these will correct several erroneous notions nesiologists, dance educators, massage early views are inaccurate. There is new about GTOs that have persisted in the therapists, physical therapists, and oth- evidence regarding the role of the GTO. dance kinesiology literature. Thus, dance ers to correctly explain the behavior of 1. A GTO responds to even weak active kinesiology teachers, researchers, and this important sensory receptor. They contractions throughout the range of health practitioners can provide accurate will also be able to explain the neural motion, although GTOs are much less information to their students, readers, and circuits and physiology underlying sensitive to passive tension than to active patients. this receptor’s role, both in dancers’ of their movements and in Marjorie Moore, P.T., M.S.(Kines), Ph.D., is an Associate Professor at the College stretches often performed by dancers. of St. Catherine, Minneapolis, Minnesota. Anatomy Correspondence: Marjorie Moore, P.T., M.S.(Kines), Ph.D., 2204 Seabury Avenue, The Golgi tendon organ is named Minneapolis, Minnesota 55406; [email protected]. after (pronounced This work was presented at the 16th Annual Meeting of the International Association Gol-jee), an Italian histologist who for Dance Medicine and Science held in West Palm Beach, Florida, USA, in October studied many types of cells 2006, and published as an extended abstract in the Annual Meeting Proceedings. with early microscopes (1878) (Fig.

85 86 Volume 11, Number 3, 2007 • Journal of Dance Medicine & Science

A tension rises, the sensory fires at a faster rate (a higher frequency of action Muscle potentials). Fibers This sensory axon (or afferent axon) is called a group Ib axon. Among the Nerve many in a nerve, the designation Branches “group I” is used for the sensory axons that have the largest diameter and fastest impulse conduction velocity.13 However, there are two types of muscle Myelinated receptors, GTOs and spindles, that B nerve axon both have these large sensory axons. So, to distinguish between them, spindle axons are called group Ia and GTO axons are classified as group Ib. In addition to the sensory axon, do GTOs also have a motor axon? In Tendon receptors, sensitivity Fibers Figure 2 Mechanism of GTO sensory to stretch can be adjusted, by means nerve activation, showing enlarged fibers of small (gamma-size) motor Figure 1 A single human Golgi tendon of a tendon, with Ib sensory axon of the that carry messages from the CNS to organ receptor (magnification x147), GTO woven between them. A, When the the spindle. However, there is no mo- located at the muscle-tendon junction. It muscle is relaxed, the tendon fibers are tor neuron to the GTO. Thus, there is consists of small bundles of tendon fibers, loose and wavy, so the Ib nerve axon is not no way to adjust the sensitivity of this with axon branches entwined compressed. No nerve signal is sent to the among them, connected to 15-20 muscle . B, When the muscle con- receptor. However, sensitivity to pe- fibers from different motor units. (Source: tracts, the tendon fibers tighten and the Ib ripheral input can be altered within the Ciaccio GV, Mem. Reale Acad. Sci., Bolo- nerve axon becomes compressed between , by descending messages gna, Italy, 1890.) them, eliciting a sensory nerve signal. from the reticular activating system of the stem.4 1). It is called a tendon organ because twitch motor units activate fewer GTOs the receptor is located at the muscle- than do fast-twitch motor units.10 GTO Reflex— tendon junction. A group of GTOs is A sensory nerve fiber or axon is en- A reflex is a neural circuit that connects found at both the proximal and distal twined between these tendon fibers.11 a with a motor neuron ends of every , totaling When the muscle is relaxed, its tendon to produce a response to the sensory 10 to 86 GTOs per muscle (counted fibers are wavy and loose, allowing the (Fig. 3). The GTO’s sensory in various cat hindlimb muscles).1-3 nerve axon to pass easily between them, Ib axon leaves the GTO capsule. It then Unlike the muscle spindles, which without being squeezed. However, travels along a peripheral nerve, such are located between or “in parallel” when muscles are active (active contrac- as the sciatic nerve, from the tendon with skeletal muscle fibers, GTOs are tile tension) or are passively stretched toward the spinal cord. This axon may located end-to-end or “in series” with (passive tension), the muscle pulls on be very long, passing from a muscle muscle fibers.4 its tendon. The tendon fibers become in the foot all the way to the spine. A single GTO receptor is large taut, squeezing the nerve axon between It enters the dorsal root, a bundle of enough (1.6 mm long x 0.1 mm wide in them12 (Fig. 2). This mechanism works sensory axons that enters each segment humans)5,6 to be seen by the naked eye. rather like a Chinese finger trap. of the spinal cord. The cell body of The GTO consists of a This compression changes the prop- this sensory nerve is located here, in a capsule, shaped like a spindle, enclosing a erties of the nerve membrane, mak- cluster called the dorsal root . small bundle of tendon fibers. This tiny ing it more permeable to ions in the The axon enters the cord, passing tendon bundle is attached to 10 to 20 environment surrounding the nerve. through the dorsal horn of gray mat- muscle fibers in humans,5 coming from Sodium ions enter the nerve, through ter. Deeper in the cord, it terminates 2 to15 different motor units7 within small pores or “ion channels,” leading in an excitatory on a short the same muscle, allowing a GTO to to nerve excitation (depolarization). (a neuron that connects “sample” tension from many parts of The harder the nerve is squeezed, the two other larger neurons). The short a muscle.8,9 Due to “unloading” effects more excitation occurs. If this electrical axon of this interneuron then goes into from non-attached motor units, GTOs potential reaches a critical threshold, the ventral horn of the spinal cord gray respond more strongly to contraction the sensory nerve will fire an action matter. There, this interneuron has an of their attached muscle fibers than to potential (a signal that can propagate inhibitory synapse onto an alpha motor contraction of the whole muscle.8 Slow- itself along the nerve’s axon). As muscle neuron cell body.14,15 Finally, these large Journal of Dance Medicine & Science • Volume 11, Number 3, 2007 87

grams, or ten times less sensitive to stretch than to contraction.24 In fact, 48% of the receptors these investigators studied did not even respond at all to maximum muscle stretch. GTO signals provide reliable infor- mation to the about the amount of muscle contrac- tion during all contraction, not just at end-range extremes. Small contractions elicited a low frequency of firing. With stronger muscle stimuli and stronger contraction, the GTO fired action potentials at a higher frequency (faster discharge rate). Its firing frequency provides a code telling the brain about the amount of contraction, or “muscle effort,” from small to large, at any Figure 3 Autogenic inhibition reflex and its circuit in the spinal cord. Input arrives via joint angle. GTOs are also sensitive to GTO’s sensory Ib axon (which has its cell body in the or DRG). It on an inhibitory interneuron, which then synapses on an dynamic changes in contraction force, so they signal rate of force change as (MN) back to the same muscle. The first synapse in the spinal cord is excitatory (+), but 25 the second synapse is inhibitory (-). The synapse at the muscle is always excitatory. In the well. In fact, the critical parameter opposing autogenic excitation reflex to the antagonist muscle (not shown), the second that GTOs signal to the CNS may be spinal cord synapse is excitatory. variation in contractile force, rather than actual force.21 The ensemble of motor neurons send their axons out of as a protective warning, to prevent tear- all GTOs from a muscle provides a the spinal cord, traveling back out the ing of the stretched muscle at end range reliable monitoring of whole muscle same peripheral nerve, returning to the of movement. This concept has been force, even during fatiguing and ec- same muscle in which the GTO recep- negated by evidence from subsequent centric contractions.26 tor was located. This circuit is known research (see next section). as a spinal (Fig. 3). (Note that Early research also credited GTOs GTO’s Spinal Reflex— this inhibitory reflex can be reversed by with the “clasp-knife reflex.” This term Autogenic Inhibition activating excitatory dur- describes the “lengthening response” A spinal reflex is a neural circuit that ing locomotion, to increase extensor or a sudden decrease in resistance to has four components: 1. a sensory support for weightbearing.16,17) passive stretch that is often seen in receptor and its sensory axon; 2. one patients with spasticity. Recent research or more synapses in the spinal cord; 3. GTO Function—Historical has shown that other high-threshold a motor neuron and its motor axon; View receptors are responsible for this phe- and 4. a muscle, or other effector organ Early research on GTOs18 investigated nomenon, not the GTO.19 such as a gland. This circuit does not only passive muscle tension (or stretch) involve the brain. in anesthetized animals. The inves- GTO Function—Modern Autogenic inhibition means “self- tigators pulled on the tendon while Concept generated inhibition.” It is the name measuring the frequency of action Later research on GTOs20 studied ac- given to the spinal reflex response that potentials from the Golgi tendon or- tive contractile muscle tension as the occurs when the Golgi tendon organ gan to assess its response. Under these stimulus, instead of passive stretch. receptor is activated, then producing conditions, GTOs did not respond at They used electrical stimulation ap- an inhibitory response in the motor all to stretch until the muscle passive plied to the muscle to cause it to con- neurons that return to the same muscle tension was very high. Near the limit tract and measured the frequency and its synergists.27 Anatomically, this of extreme tension, the Golgi tendon of action potentials from the Golgi circuit consists of: 1. the GTO recep- organ would fire a burst of action tendon organ to assess its response. tor and its sensory Ib axon, passing potentials. This burst would alert the Under these conditions, the GTO was through a peripheral nerve to the central nervous system of extreme ten- more sensitive to active than to passive spinal cord; 2. an excitatory synapse sion in the muscle. forces.20,21 In fact, GTOs can respond onto a short ; 3. This early result lead to the idea that to contraction of a single muscle fi- which then has an inhibitory synapse the only role of the GTO was to sense ber.22,23 In cats, detection thresholds for onto alpha motor neurons that return excessive amounts of muscle stretch, active tension are 2 to 25 grams, while to the same muscle where the GTO and to the belief that GTO signals serve for passive tension, they are 20 to 200 is located. Thus, 88 Volume 11, Number 3, 2007 • Journal of Dance Medicine & Science triggers GTOs to reflexively produce use the GTO circuit and its reflex contraction, so there would be little or inhibition, or a reduction in excit- effects. The goal of safe stretching is no firing from the GTO receptor of ability of that same muscle and its usually to provide maximal relaxation the stretched muscle. At the extreme synergists.28 Since this circuit contains of the muscle during stretch so that its of end range, there may be some two synapses,29 it is called a disynaptic own contraction does not oppose the GTO response to the muscle’s passive reflex. (Circuits with only one synapse intended lengthening. Let us consider stretch tension. When summation of are called monosynaptic.) An opposite two kinds of hamstring stretching, inputs occurs at the motor neuron, excitatory effect is produced in antago- both of which originated from physi- it receives inhibitory signals from the nist motor neurons, called autogenic or cal therapists. These techniques come brain, attempting to induce voluntary reciprocal excitation.28 from a therapeutic approach known as relaxation. It receives little excitation What is the function of the GTO’s PNF or proprioceptive neuromuscular from the muscle spindle receptor’s autogenic inhibition reflex? It is not facilitation.32 This theory attempted axon, and it receives no signal or some correct that GTO input to the spinal to use knowledge of proprioceptor added inhibition from the GTO. So cord suppresses all activity in its target function (as of the 1950s) to develop the combined effect is to inhibit the motor neurons, totally preventing techniques for facilitating muscle motor neuron from firing, leading to a muscle contraction, leading to auto- contraction in muscles weakened by relaxed muscle. This stretch technique matic muscle relaxation. In reality, mo- the polio epidemic of that era. PNF is therefore a safe and gentle stretch. tor neurons receive hundreds of inputs also included descriptions of a few in- from a variety of limb sensory recep- hibitory techniques,33 which have now CR Stretch tors and from higher brain centers.30 been adapted for muscle stretching to Contract-relax stretch of the ham- Each input produces a tiny excitatory increase flexibility. strings begins in a stretched position of (EPSP) or inhibitory (IPSP) signal. The Let us consider three kinds of ham- hip flexion and knee extension, usually sum of all these inputs will determine string stretching techniques and the at the end of current range of motion. whether the motor neurons will fire or role that GTOs play in each one. The During phase 1, an active contraction not. three stretch techniques are: 1. static of the stretched hamstring muscles is One signal from a GTO alone is not stretch, 2. contract-relax (CR) stretch, performed voluntarily (either isometric enough to control the motor neuron’s and 3. contact relax with agonist con- or concentric). In phase 2, the ham- response. Input from a GTO only traction (CRAC) stretch.34 string muscles are voluntarily relaxed, partially reduces the excitability of the with further stretch applied passively motor neuron and its muscle.31 Signals Static Stretch (by gravity, a partner, or pulling the from many GTOs, firing repetitively, Static stretch involves positioning the leg closer to the face using the hands). are needed to have a chance of sum- limb so that the target muscle is in a This cycle of contraction and relaxation mating and producing a response in position of maximal elongation. The with stretch can be repeated multiple the motor neuron. The autogenic reflex name comes from the fact that the times. This technique is a modification does not “turn off” the muscle, prevent- joint remains in an essentially static or of the PNF inhibitory technique called ing its contraction and forcing the unchanging position (as opposed to “hold-relax”32 (Fig. 4). muscle to relax completely. Instead, the the old ballistic stretches that involved Summary: GTO just makes it slightly less likely bouncing movement at the joint). Phase 1: hamstring contraction (in a that its host muscle will contract. This limb position is then maintained, stretched position) usually for 30 seconds, during which Phase 2: hamstring and whole leg Relevance to Dance Science, a stretch is felt. An attempt is made relaxation (and more stretch) Dance Education, and Manual to voluntarily relax the muscle during In this stretch, what role does the Therapy the stretch. GTO play? Some teachers incorrectly Knowledge of GTO receptors and The static stretch primarily attempts state that the phase 2 muscle relaxation their reflex effects is useful in dance, to avoid exciting the muscle spindle is produced because of GTO activation primarily for explaining the effects of receptor. This receptor is sensitive to from the initial phase 1 contraction. It muscle stretching techniques, as well as very small amounts of stretch, par- is true that a relaxation occurs, which understanding dancers’ sense of body ticularly if they are applied rapidly, as improves the stretch. However, it is position in space, and their “sense of in bouncing stretches. So by holding unlikely that the GTO produces it. effort” when moving. the limb still, or moving it very slowly During phase 1, hamstring GTO toward increasing stretch, an attempt activity would occur during the phase GTO Role in Muscle Stretching is made to reduce the magnitude of the 1 contraction and it would reflexively Physical therapists who treat dancers spindle’s response, thereby reduce on-going contraction during employ many different kinds of stretch- keeping the muscle more relaxed. that phase. However, this inhibitory ing techniques, as do dancers and their What role does the GTO play in function is over-ridden by the volun- teachers. Several stretching variations this stretch technique? It probably plays tary effort to contract the hamstrings. have been developed that purport to very little role. There is no active muscle Descending messages from the brain Journal of Dance Medicine & Science • Volume 11, Number 3, 2007 89

Figure 4 Contract relax (CR) stretch of the hamstrings. Phase I is Figure 5 Contract relax with agonist contraction (CRAC) stretch. a voluntary isometric hamstring contraction. Phase 2 is a voluntary Phase I is a voluntary hamstring contraction. Phase 2 is a voluntary relaxation of the hamstrings, with more passive hamstring stretch. relaxation of the hamstrings, together with a voluntary contraction (Solid arrow = active contraction, dashed arrow = passive stretch of the quadriceps, and more passive hamstring stretch. (Solid arrows force.) = active contractions, dashed arrow = passive stretch force.) provide more facilitation to the motor at the onset. In phase 1, a voluntary GTOs have on the hamstrings during neurons than the inhibition coming contraction of the stretched hamstring phase 2? These quadriceps GTOs will from the GTOs. muscles is performed, exactly as in CR inhibit the quadriceps motor neu- In phase 2, once the contraction stretch. In phase 2, the hamstrings vol- rons, but they will have the opposite ends, the hamstrings relax and the untarily relax and further stretch occurs effect in the antagonist hamstring GTO ceases its firing activity. Thus it (by means of an outside force). motor neurons, leading to excitation cannot influence the degree of subse- At the same time that the ham- of hamstring motor neurons. This quent muscle relaxation. In fact, there strings relax, the opposing muscles excitation may not be sufficient to is a brief post-contraction desensitiza- (quadriceps) are voluntarily contracted. reach the threshold to cause an active tion of the GTO.35 This hamstring [The quadriceps is theagonist because it contraction. But the GTO reflex tends relaxation is more than a voluntary acts to increase the desired hip flexion to prevent the intended relaxation letting go. There is a real inhibition movement. In contrast, the hamstrings of the stretched hamstrings. Their of hamstring reflex excitability that are the antagonist because they oppose motor neurons are also being excited has been measured.36 The magnitude the desired hip flexion movement.] by the stretched hamstring muscle of this effect is large (mean 83.3% This stretch is a modification of the spindles, so there are two forces act- depression at 0.1 to 1.0 second post- PNF inhibitory technique of “slow ing to oppose the intended hamstring contraction). But this inhibition lasts reversal-hold-relax”32 (Fig. 5). relaxation. Rather than being help- less than ten seconds after the contrac- Summary: ful, GTOs are counterproductive in tion ends. Phase 1: hamstring contraction (in CRAC stretching, serving no useful Rather than being produced by the stretched position) purpose. GTO, some other mechanism for post- Phase 2: hamstring relaxation + quad- What then accounts for the relax- contraction muscle relaxation must be riceps contraction ation that is experienced in phase 2 of sought. Investigations have provided In this stretch, what role does the the CRAC stretch? It is another spinal evidence that Renshaw interneurons GTO play? As in CR stretching, dur- circuit called reciprocal inhibition. of the spinal cord are also not respon- ing phase 1, hamstring GTOs will be During the quadriceps contraction, sible.37 More likely explanations are activated by the contraction, but their not only are its GTOs active, but so messages from other high-threshold effects are over-ridden by the voluntary are its muscle spindles. Spindles can sensory receptors residing in connective contraction. And during phase 2, the be excited not only by stretch, but also tissues of the muscle and hip joint. An hamstrings are relaxed, so their GTOs by contraction (provided that there is additional possibility is pre-synaptic will not be active and will have no ef- normal gamma motor neuron activity inhibition between competing sensory fect. The unique feature of the CRAC that tightens the spindles to prevent afferents as their terminal endings ar- stretch is that the quadriceps muscles them from being “unloaded” or slack- rive in the spinal cord.4,38 are active in phase 2. Their GTOs will ened by the shortening muscle).39,40 be activated leading to reflex suppres- This incoming spindle sensory input, CRAC Stretch sion of quadriceps contraction. This ef- arriving via Ia sensory axons, activates Contract-relax with agonist contrac- fect will be overcome by the voluntary a small interneuron in the spinal tion stretch begins the same way as CR messages to the quadriceps muscle. cord, called the Ia reciprocal inhibi- stretch. The limb is in end-range stretch But what effect will the quadriceps tory interneuron, or Ia interneuron for 90 Volume 11, Number 3, 2007 • Journal of Dance Medicine & Science short. The synapse between the muscle tion of the proprioception sensory bral cortex. Such knowledge is critical, spindle Ia axon and the Ia interneuron receptors, but also on their pathways both for motor learning of new move- is excitatory. In turn, this Ia interneu- up the spinal cord to the brain cortex, ments and for monitoring on-going, ron synapses with motor neurons of as well as on the brain making sense well-learned movements for errors in the opposing hamstring muscle group. out of these incoming messages. This limb trajectory or force. This synapse is inhibitory. And so this interpretive process happens in the Functionally, what role does the reciprocal inhibitory circuit can inhibit parietal lobes of the somatosensory GTO play in proprioception? It pro- hamstring motor neurons from firing, cortex.4 vides information to the brain about keeping the hamstring muscle relaxed Historically, researchers did not both movement direction and move- during phase 2 of the stretch. think that proprioceptive messages ment intensity (“sense of effort”). It should be noted that all of these reached consciousness, because their When we move a certain direction, effects are short-lasting. Most neural signals couldn’t be recorded on the particular groups of muscles contract to phenomena last only a few milli- surface of the brain’s sensory cortex, move us there. Their receptors (GTOs seconds (thousandths of a second). where touch signals were recorded.42 and spindles) fire messages to the brain. There is no evidence that reciprocal However, later research revealed that When your brain knows which muscles inhibition lasts longer than the agonist proprioceptive messages do reach the are active, it can figure out whether (quadriceps) contraction. Similarly, cortex, but they reach cells buried deep limbs are flexing or extending (move- there is no evidence that GTO auto- in a groove (central sulcus) on the brain ment direction). When babies appear genic inhibition lasts longer than the surface.43 The sensory cortex area is to be randomly flailing their limbs, contraction of its parent muscle. The located in the post-central gyrus,44 they are actually teaching their nervous only exception may be muscle spindle specifically on its anterior wall, crown, system how to interpret limb sensory discharge. There is some evidence that and posterior wall. This brain strip has input. Their eyes see where their limb spindle firing may outlast its muscle separate zones for signals from each is and they compare that input to the contraction.41 This phenomenon is body region, with legs represented at proprioception coming from the limbs. called “post-contraction sensory dis- one end of the strip (in the longitudinal Eventually, the brain can then interpret charge,” or PCSD. It may be respon- fissure between right and left lobes) these signals without vision. sible for the sensations of movement then trunk, arms, and hands succes- Secondly, when we perform more that sometimes persist after prolonged sively located along the strip, ending vigorous movements, the intensity of exercise. For example, when you stop with face sensations at the other end of muscle contractions increases. This ac- ice skating, you may feel like you are the strip (at the lateral fissure), thereby tive tension is very effective at stimulat- still sliding for the first few steps after creating a “body map.”45,46 The sensory ing GTO receptors. So the harder we you are on solid ground. cortex actually includes four parallel contract our muscles, the more firing body maps (areas 1, 2, 3a, 3b),47 with there is from the GTO receptors resid- Proprioception each map specializing in different sen- ing there. This information reaches This term literally means “self-sens- sory modalities, with area 3a specialized our brain, where it is combined with ing.” It describes our ability to sense for muscle proprioception, while other copies of descending commands from the position of our own body and its areas receive input about touch or joint the brain’s motor centers, together individual body segments in space position. Muscle spindle48 and GTO interpreted as movement “effort.” (even with our eyes closed). This abil- inputs49 are both known to reach cortex In conclusion, GTOs are muscle ity uses information from the sensory area 3a, deepest in the central sulcus. sensory receptors that sense muscle receptors located in our muscles and Signals from both passive and active force. They produce important reflexes tendons (spindles and GTOs), joint movements can be recorded here,50 as that control muscle tension levels. capsules and ligaments, connective tis- well as signals related to both muscle Although they are often included in sues, skin (especially soles of the feet), force and movement direction (flexion descriptions of flexibility physiology, and ear balance organs ( and versus extension).51-53 current knowledge indicates that they utricle), all of which inform our central In contrast, unconscious (really sub- are probably not involved in static or nervous system of what is going on in conscious) proprioception means that PNF-based stretches. When writing the periphery. your brain can use this sensory infor- about flexibility training, the use of Our brain is capable of both con- mation to coordinate your movements, current concepts about GTOs will en- scious and un-conscious propriocep- without consciously thinking about it. hance the credibility of dance kinesiol- tion. Conscious proprioception means This process occurs in the cerebellum, ogists, teachers, and therapists. Despite that we are consciously aware of our which receives input from GTO and the irrelevance of GTOs to stretching, body position. If asked, you could other proprioceptor axons ascending these receptors are still very useful to describe your position verbally, or you the spinal cord.54,55 By “knowing” dancers. They tell our where our could voluntarily mimic a positioned where your limb segments are now, limbs are in space, which muscles are limb using your opposite limb. This your brain can plan future movements. active, and how much effort is being ability depends not only on the func- This process does not require the cere- exerted. They are absolutely necessary Journal of Dance Medicine & Science • Volume 11, Number 3, 2007 91 when learning new motor skills, and motor neurons that control the man Golgi tendon organs as studied in perfecting execution of previously muscle containing the GTO recep- by three-dimensional reconstruction. acquired skills. tor. It reduces the likelihood of J Neurocytol. 1988;17:27-41. muscle contraction. 7. Binder MD, Osborn CE: Interac- Summary and Conclusions • PNF-based stretching techniques tions between motor units and Golgi tendon organs in the tibialis This article has attempted to cor- are useful ways to increase flexibility posterior muscle of the cat. J Physiol. rect some misperceptions about the in dancers. However, GTOs seem to 1985;364:199-215. function of the Golgi tendon organ play little useful role in responding 8. Binder MD: Further evidence that (GTO): to various stretching techniques. the Golgi tendon organ monitors • GTOs do not serve only a protective Other sensory receptors and spinal the activity of a discrete set of motor role, to prevent muscle tears, nor do mechanisms are likely involved. units within a muscle. Exper Brain they function only at extreme joint • During dance and other normal Res. 1981;43(2):186-92. end range. movement, GTOs provide con- 9. Crago PE, Houk JC, Rymer WZ: • stantly updated information to Sampling of total muscle force by They are not responsible for the tendon organs. J Neurophyiol. “clasp-knife reflex” or “lengthening the brain for conscious awareness of body position and for un-con- 1982;47:1069-83. reaction.” 10. Horcholle-Bossavit G, Jami L, Petit • Autogenic inhibition produced by scious coordination of movement. R, et al: Ensemble discharge from GTOs does not completely turn They also provide awareness of Golgi tendon organs of cat pero- off contraction in the receptor’s which muscles are active and of the neus tertius muscle. J Neurophysiol. host muscle. It does not produce amount of effort. 1990;64:813-21. complete relaxation or release of • Therefore, GTOs are involved in 11. Schoultz TW, Swett JE: The fine tension. the control and refinement of move- structure of the Golgi tendon organ. ment skills in dancers, without the J Neurocytology. 1972;1(1):1-25. In contrast, the following is a sum- dancer even having to think about 12. Swett JE, Shoultz TW: Mechanical mary of the structure and main func- it. transduction in the Golgi tendon tions of the GTO: organ: a hypothesis. Arch Ital Biol. • GTOs are sensory receptors located Acknowledgments 1975;113:374-82. at the muscle-tendon junction at 13. Lloyd DPC, Chang HT: Afferent The author would like to thank Donna fibers in muscle . J Neuro- both ends of skeletal muscles. Krasnow, M.S., and Tom Welsh, Ph.D., physiol. 1948;11:199-207. • They monitor muscle force, unlike for their helpful comments on previous 14. Watt DGD, Stauffer EK, Taylor A, spindles which monitor muscle drafts of this manuscript. et al: Analysis of muscle receptor length (stretch). connections by spike-triggered aver- • GTOs are most sensitive to active References aging: I. Spindle primary and tendon contractile tension, as during move- 1. Barker D: The structure and distribu- organ afferents. J Neurophysiol. ment. tion of muscle receptors. In: Barker 1976;39:1375-92. • They can also detectpassive tension, D: Symposium on Muscle Receptors. 15. Eccles JC, Eccles RM, Lundberg A: but only at extremes of stretch. Hong Kong: Hong Kong Univ. Press, Synaptic actions on motoneurons • They respond vigorously even dur- 1962. pp. 227-240. caused by impulses in Golgi tendon ing small contractions at all joint 2. Eldred E, Bridgman CF, Swett JE, organ afferents. J Physiol Lond. Eldred B: Quantitative comparisons 1957;138:227-52. positions, not just at extreme muscle of muscle receptors of the cat medial 16. Pearson KG: Proprioceptive regu- lengths. gastrocnemius, soleus, and extensor lation of locomotion. Curr Biol. • GTOs produce autogenic inhibition digitorum brevis muscles. In: Barker 1995;5:786-91. of their host muscle and recipro- D: Symposium on Muscle Receptors. 17. Pearson KG, Collins DF: Reversal cal excitation of antagonists. In Hong Kong: Hong Kong Univ. Press, of the influence of Ib afferents contrast, spindles produce stretch 1962. pp. 207-213. from plantaris on activity in model reflex excitation of their host muscle 3. Scott JJA, Young H: The number and gastrocnemius activity during lo- and reciprocal inhibition of antago- distribution of muscle spindles and comotor activity. J Neurophysiol. nists. tendon organs in the peronei muscles 1993;70:1009-17. • Autogenic inhibition is a reflex of the cat. J Anat. 1987;151:143- 18. Matthews BHC: Nerve endings in response produced by the GTO’s 55. mammalian muscle. J Physiol Lond. 4. Kandel ER, Schwartz JH, Jessell TM: 1933;78:1-33. sensory (Ib) axon, designed to Principles of Neural Science (4th ed). 19. Cleland CL, Rymer WZ: Neural maintain constant tension in its New York: McGraw Hill, 2004. mechanisms underlying the clasp- host muscle. This reflex inhibition 5. Bridgman CF: Comparisons of the knife reflex in the cat. I. Character- helps to counteract the stretch reflex structure of tendon organs in the , istics of the reflex. J Neurophysiol. excitation (produced by spindles) cat, and human. J Compar Neurol. 1990;64:1303-18. from the same muscle. 1970;138:369-72. 20. Houk J, Henneman E: Reponses of • This reflex acts to partially inhibit 6. Nitatori T: The fine structure of hu- Golgi tendon organs to active con- 92 Volume 11, Number 3, 2007 • Journal of Dance Medicine & Science

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