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Sports Biomechanics
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Strength training
a
Gordon Chalmers
a
Department of Physical Education, Health and Recreation ,
Western Washington University , Bellingham, WA, USA
Published online: 20 Jul 2007.

To cite this article: Gordon Chalmers (2002) Strength training, Sports Biomechanics, 1:2, 239-249,
DOI: 10.1080/14763140208522800

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 Do Golgi Tendon Organs Really Inhibit Muscle
Activity at High Force Levels to Save Muscles from
Injury, and Adapt with Strength Training?

GORDON CHALMERS
Downloaded by [Linköping University Library] at 22:47 18 December 2014

ABSTRACT
Introductory textbooks commonly state that Golgi tendon organs (GTOs) are
responsible for a reflex response that inhibits a muscle producing dangerously
high tension (autogenic inhibition). Review of the relevant data from animal
studies demonstrates that there is wide variability in the magnitude of, and even
the presence of, GTO autogenic effects among locomotor hindlimb muscles,
and that data on GTO effects under conditions of voluntary maximal muscle
activation are lacking. A single available study on GTO function in humans,
during a moderate contraction, surprisingly shows a reduction in autogenic
inhibition during muscle-force production. Further, it is not possible to find
experimental evidence supporting the idea that strength training may produce
a decrease in GTO mediated autogenic inhibition, allowing greater muscle
activation levels and hence greater force production.

Keywords: GTO, adaptation, autogenic inhibition, motoneuron, human, animal.

INTRODUCTION
Introductory exercise physiology, biomechanics, and strength and conditioning
textbooks that discuss Golgi tendon organ (GTO) function usually state that,
when excessively high muscle forces are detected by the tendon organ, a reflex
inhibition of the same muscle results in an attempt to save the muscle from
injury during the very high forces (Table 1). This proposed reflex pathway is
shown in Figure 1. The excitatory signal for contraction of the muscle initiated
by the brain (A) is carried from the spinal cord to the muscle by the motoneuron
(B). The force produced by the active muscle is detected by the Golgi tendon
organ (C) and sends signals back to the spinal cord (D). The sensory signals act
via a Ib inhibitory interneuron (E) to reduce the activation of the motoneuron
(B) to relax the same active muscle and prevent the potentially damaging high
forces from being maintained. The goals of this brief review are to examine
data on GTO reflex function to determine whether it is correct to state that: (1)

Department of Physical Education, Health and Recreation,

Western Washington University, Bellingham WA, USA

Sports Biomechanics Vol.1 (2) 239-249

 240 GORDON CHALMERS

Golgi Jendon organs inhibit muscle activity at high force levels, to potentially
save muscles from injury, and (2) muscle inhibition by the Golgi tendon organ
reflex adapts following strength training to facilitate the production of high
forces.

Table 1 Sample of statements made in textbooks regarding the function of

Golgi tendon organs when: (1) a high muscle force is produced, and (2) how
tendon organ reflex function adapts with strength training.

Source Stated effects of Golgi tendon organ activation and

adaptation
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Powers and Howley, 2001 (1) GTOs serve as 'safety devices' that help prevent
excessive force during muscle contraction -
pg. 152.
(2) Inhibitory influences of the GTO could be gradually
reduced in response to strength training - p. 153,
reference: Wilmore and Costill, 1993.
Brooks, Fahey, White and (1) When the forces of muscle contraction and the
Baldwin, 2000 forces resulting from external factors sum to the
point where injury to the muscle, tendon or bone
becomes possible, then the GTOs cause inhibitory
postsynaptic potentials on the cell body of the
agonistic motor units - p. 391.
(2) The process of minimising the influence of GTOs is
termed disinhibition. Practising disinhibition
appears to be part of athletic training - p. 392, no
reference provided.
Kreighbaum and (1) The GTOs' response to stretch is to inhibit the
Barthels, 1996 contraction of the associated muscle - p. 73.
(2) Decreasing the sensitivity of GTOs through strength
training has been proposed - p. 74, reference:
Komi, 1992.
Fleck and Kraemer, 1997 (1a) If the tension becomes great enough that damage
to the muscle or tendon is possible, inhibition of
the activated muscle occurs - p. 63.
(1b) Inhibition of muscle action by reflex protective
mechanisms, such as that provided by the Golgi
tendon organs, has been hypothesised to limit
muscular force production - p. 141.
(2a) It may be possible through resistance training to
learn to disinhibit the effects of the GTOs - p. 63,
no reference provided.
(2b) Neural adaptation to strength training includes an
inhibition of protective mechanisms of the muscle
(i.e. Golgi tendon organs) - p. 140, no reference
provided.
 DO GOLGI TENDON ORGANS REALLY INHIBIT MUSCLE ACTIVITY 241

(2c) Resistance training may cause voluntary inhibition

of protective mechanisms - p. 141, reference: Ikai
and Steinhaus, 1961.
(2d) After a period of plyometric training the inhibitory
effects are reduced - termed disinhibition - and
force during stretch-shortening cycle increases as a
result - p. 146, reference: Schmidtbleicher et al.
1988.
Baechle and Earle, 2000 (1) The GTOs inhibitory process is thought to provide
a protective mechanism from development of
excessive tension - p. 20.
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(2) The ability of the motor cortex to override this

inhibition may be one of the fundamental
adaptations to resistance training - p. 20,
no reference provided.

A/B / /
,—,
/Aj I <
AMB/ /^kr
(D)
Gogli tendon
v
organ signal to
the spinal cord
1
f
1
Brain excitory signal
to activate
(A) muscle

Ib inhibitory
interneuron
^*^f Motoneuron
/ activating
/ muscle

\ \ \ \ Gogli

VSSL organ"

Figure 1 Schematic of the basic concept of Golgi tendon organ (GTO) function,
illustrated for the gastrocnemius muscle (See text for details). Note that this
schematic has been simplified in numerous ways, including diagramming the
excitatory input from the brain as only going directly to the motoneuron, omitting
other inputs to the inhibitory interneuron and to the motoneuron, and showing only
the effects of the reflex on the muscle producing the force.
 242 GORDON CHALMERS

PART 1: DO GOLGI TENDON ORGANS INHIBIT MUSCLE

ACTIVITY AT HIGH FORCE LEVELS, TO POTENTIALLY
SAVE MUSCLES FROM INJURY?
There are numerous research studies demonstrating GTO mediated reflex
inhibition of an active muscle (termed autogenic inhibition). This was first
clearly elucidated in 1950 by Granit (1950) with respect to cats, and verified
numerous times since then (e.g. Eccles et al., 1957; Nichols, 1999). Additional
data, however, bring to light numerous concerns when extrapolating these
findings under experimental conditions into a general statement of a GTO
reflex protective function in an intact, naturally operating neuromuscular system.
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First, the 'classic' inhibitory reflex does not operate for all motoneurons; second,
the inhibition observed declines extremely rapidly under some conditions; and
third, limited human data have indicated that reflex inhibition may decrease
with a contraction.

The Breadth of the Presence of the 'Classic' Inhibitory Reflex

Eccles et al. (1957) found that while autogenic inhibition was present in most
cat hindlimb extensor muscles examined (although only in a portion of most
of those muscles), it was largely absent in hindlimb flexors. Specifically, for
extensor motoneurons examined across many cats, 5 of 14 (35%) of quadri-
ceps, 26 of 63 (41%) of triceps surae (gastrocnemius and soleus), 10 of 10 of
plantaris, and 15 of 18 (83%) of flexor digitorum longus motoneurons exhibited
autogenic inhibition. In the two flexor muscles examined, only 4 of 52 (8%) of
biceps-semitendinosus motoneurons, and 2 of 36 (6%) of pretibial flexor
motoneurons (tibialis anterior and extensor digitorum longus) showed auto-
genic inhibition. Further, this variation existed both across animals (some had
virtually no autogenic inhibition in the extensors, while others demonstrated it
often), and within animals (a wide range in the strength of autogenic inhibition
could be observed across the motoneurons for a given extensor muscle in an
animal). In contrast to the sparse flexor autogenic inhibition reported by Eccles
et al. (1957), Green and Kellerth (1967) reported autogenic inhibition in almost
all of 37 pretibial flexor motoneurons examined during muscle contraction.
Surprisingly, however, it was found that the autogenic inhibition was maximal
when the flexor muscle was at a slack length. When the muscle was lengthened,
the magnitude of the observed autogenic inhibition during an isometric con-
traction was reduced. Furthermore, the magnitude of the autogenic inhibition
decreased to the point at which there was no inhibition observed for the longest
muscle length tested (still within the normal physiological range of length). In
contrast, others (Granit et al., 1966) found that when cat hindlimb extensor
motoneurons were held in a stretched position, the muscle contractions roduced
even stronger autogenic inhibition than when in a shorter position.
In the peroneal muscles of the cat, muscle contraction had an unexpected
autogenic excitation effect, rather than inhibition (Kouchtir et al., 1995). The
basis for this excitation has been hypothesised to be muscle spindle activation,
although evidence also indicated the possibility that GTO mediated autogenic
excitation may have played a role.
 DO GOLGI TENDON ORGANS REALLY INHIBIT MUSCLE ACTIVITY 243

In summary, most of the data available on GTO autogenic inhibition in

mammals has come from the cat hindlimb because that is the experimental
model system most widely used for motor unit studies in mammals (Jami,
1992).
Although limited, these data indicate that an all-encompassing statement
such as 'muscle contraction induced activation of Golgi tendon organs results in
inhibition of muscle activity' is not possible. There is clearly a wide variability
in magnitude, and even presence of GTO autogenic effects among locomotor
limb muscles. It is not known how these results may be extrapolated to non-
locomotor muscles, even in the cat, because GTO reflex function in the cat
hindlimb has been strongly related to the locomotor function of the muscles
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(Pratt, 1995). Furthermore, the available data on reflex effects of GTO activation
have been collected at submaximal contraction levels (Granit, 1950; Granit et
al., 1966; Green and Kellerth, 1967), or has mimicked muscle contraction by
stimulating sensory nerves directly (Eccles et al., 1957), so extrapolation to
maximal muscle activation levels is speculation (also see 'Human Data' below).

Declines in Inhibition
In the studies discussed above (e.g. Granit et al., 1966; Green and Kellerth,
1967), the muscle contraction used to elicit autogenic inhibition was typically
a muscle twitch caused by a single or double stimulus. The production of
muscle force is normally achieved by a rapid series of action potentials, allow-
ing the twitch force response to one action potential to add on to the twitch
force responses from the previous action potentials. The overlapping and
addition of the twitch force responses is known as tetanus. The autogenic
inhibition observed in the cat medial gastrocnemius during isometric partially
fused tetanic contractions lasting 0.5-4 seconds at 10-50% of total muscle
twitch force was examined by Zytnicki et al. (1990). While there was signifi-
cant autogenic inhibition following the first stimulus and twitch in 85% of the
medial gastrocnemius motoneurons examined, the inhibition was reduced for
the second stimulus, and thereafter during the contraction autogenic inhibition
was not observed. The autogenic inhibition had faded within approximately
100 milliseconds following the start of the contraction, despite the fact that it
was demonstrated that the GTOs continued to fire action potentials due to the
contraction stimulus. In the remaining medial gastrocnemius motoneurons
examined there was no autogenic inhibition observed.
In contrast, when an isometrically contracting cat muscle is stretched
(eccentric contraction) and held at the longer length for several hundred millisec-
onds to increase muscle tension and stimulate GTOs, motoneuron inhibition is
maintained for the duration of the stretch (Nichols, 1999). It should be noted
that in the Nichols (1999) study, stretch of the medial gastrocnemius or the lat-
eral gastrocnemius was observed to induce inhibition of soleus motoneurons
for the duration examined. The time course of autogenic inhibition of medial
or lateral gastrocnemius motoneurons was not reported, but is expected to be
of a similar duration to that reported for the soleus inhibition.
In summary, under the isometric contraction condition tested (0.5-4 seconds)
 244 GORDON CHALMERS

(Zytnicki et al., 1990) the potential for the GTO autogenic reflex to reduce
muscle tension to prevent injury following the initial milliseconds of the con-
traction is largely impaired, or non-existent. During an eccentric contraction,
however, the potential for autogenic inhibition is maintained for the duration
tested (<1 second) (Nichols, 1999).

Human Data
Virtually all of the knowledge about GTO reflex function is derived from animal
studies because most of the measurement techniques used are applicable only
to animal experiments. One study performed in humans sheds significant light
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on GTO reflex function during voluntary contractions (Fournier et al., 1983).

Compared to the levels of GTO autogenic inhibition found at rest, a 'medium'
force contraction of the triceps surae (gastrocnemius and soleus) depressed
autogenic inhibition of soleus motoneurons. This finding of reduced autogenic
inhibition during a voluntary contraction is in direct opposition to an expected
increase in, or at least maintenance of, autogenic inhibition during a contrac-
tion to protect a muscle from injury. The control of the reflex inhibition was
believed to come from supraspinal (i.e. the brain) sources (Fournier et al.,
1983).

The Clasp-Knife Reflex

Recent evidence demonstrates that GTOs are not involved in the 'clasp-knife'
reflex. In some specific animal studies, and in some spastic human limbs, a
lengthening of a contracted muscle has been observed to result in a sudden
decrease in muscle tension (Duysens et al., 2000). For example, lengthening of
the knee-joint extensors induced by joint flexion produced a drop in tension
allowing the joint to rapidly flex further. The action was termed the 'clasp-
knife' reflex due to flexion of the joint being analogous to the folding of a
pocketknife (Cleland and Rymer, 1990). Originally this reflex was attributed to
GTO firing being activated at a high level of muscle tension as the contracted
muscle was stretched (Jami, 1992), however, GTO involvement has been ruled
out (Cleland and Rymer, 1990; Jami, 1992).

Summary
Part 1 of this review has focused on the effect of muscle contraction, sensed by
the GTOs, on the motoneurons of the contracting muscle in cats and humans.
The literature on GTO reflex function is, however, much broader and includes
additional information on the effect of GTO activation on muscles other than
the contracting muscles, and the effect of other neural systems to excite or
inhibit GTO reflex pathways (see reviews by Duysens et al., 2000; Jami, 1992;
McCrea, 1986). The current consensus is that GTO reflexes are not a simple
predictable pathway that can be summarised in a single statement such as
'GTO activation inhibits muscle contraction'. Rather GTO activation may have
variable effects resulting from the task, the muscle activated, and input from
 DO GOLGI TENDON ORGANS REALLY INHIBIT MUSCLE ACTIVITY 245

other neural sensory and brain systems (Duysens et al., 2000; Jami, 1992;
McCrea, 1986). The wide variability in GTO reflex autogenic action means
extrapolation of results from very controlled experimental conditions in animal
studies to human movement is frauight with problems. For example, in many
animal studies a single muscle largely isolated from the limb is contracting
with a twitch or even a tetanus whereas in human movement multiple sensory
and descending systems are active and interacting. (Duysens et al., 2000).

PART 2: DOES MUSCLE INHIBITION BY THE GOLGI TENDON

ORGAN REFLEX ADAPT FOLLOWING STRENGTH TRAINING
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TO FACILITATE THE PRODUCTION OF HIGH FORCES?

It is commonly stated that strength training may produce a decrease in GTO
mediated autogenic inhibition, allowing greater muscle activation levels and
hence greater force production (Table 1). To examine this idea, the sources of
information used to support this claim, when provided by the textbooks cited
in Table 1, will be individually examined. Then, other pertinent data will be
reviewed.

Evidence from Studies Cited in Table 1, Parts (2)

Powers and Howley (2001), citing Wilmore and Costill (1993), stated that it is
possible that inhibitory influences of the GTO could be gradually reduced in
response to strength training, although Wilmore and Costill asserted that this
idea is speculation (p. 91 in Wilmore and Costill, 1993). Similarly, Kreighbaum
and Barthels (1996) cited a proposal (not experimental evidence) by Komi (1992)
that when inhibitory force feedback from the GTO can be decreased, muscle
stiffness can be increased to enhance explosive force production following
strength and power training.
Evidence that Fleck and Kraemer (1997) used to indicate that resistance
training may produce inhibition of the GTO protective mechanism came from
a hypnosis study by Ikai and Steinhaus (1961) and plyometric studies reported
by Gollhofer et al. (1987) and Schmidtbleicher et al. (1988).
Ikai and Steinhaus (1961) examined the force produced during forearm
flexion while in a normal and a hypnotic state, for untrained and highly resis-
tance trained individuals. Fleck and Kraemer reported that Ikai and Steinhaus
found that, compared to the normal state, force production while under hypnosis
increased 17% for the non-resistance trained subjects, but failed to increase for
the trained subjects. However, examination of the Ikai and Steinhaus article
(1961), reveals that there was only one trained subject. Therefore, conclusions
comparing trained versus untrained people are questionable based on the small
sample. Further, Ikai and Steinhaus described the single trained subject as
being sceptical of the experiment, and making an 'exceptional effort' on his
control pre-hypnosis pulls. This left very little opportunity for further improve-
ment and raises the possibility of high fatigue levels reducing performance
when tested subsequently under hypnosis. Further, while Ikai and Steinhaus
(1961) concluded that the removal of 'psychological' inhibition (by hypnosis
 246 GORDON CHALMERS

or strength training) is able to enhance strength expression, they never discussed

GTOs in their article, or any other potential sources of the 'psychological'
inhibition. Hence there is no evidence produced by Ikai and Steinhaus (1961)
that any strength inhibition (and subsequent removal with strength training) is
mediated by GTOs. Concerns of not randomising the sequence of treatments
to the subjects, the subjects not being blinded to their treatment group, and cer-
tainty and consistency of the hypnotic states induced add to the inability to
draw conclusions from the hypnosis study.
It has been observed that in untrained subjects performing a plyometric
jump there is a significant reduction in ankle plantar flexor muscle activation
immediately prior to and following the time of foot contact (Gollhofer et al.,
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1987). Fleck and Kraemer (1997) stated 'Gollhofer (1987) has attributed this to
a protective mechanism caused by the Golgi tendon organ reflex acting during
sudden, intense stretch loads to reduce the tension in the musculotendinous
unit during the peak force of the stretch-shortening cycle' (p. 146). The last
sentence of the Gollhofer article (1987) stated, 'Functionally, this reduction is
suggested to cause reduced stiffness and to protect the tendomuscular system
in overload conditions' (p. 705). Note that the statement by Gollhofer quoted
previously, and the entire article, actually lacks any mention of GTOs and
provides no explanation for the inhibition in muscle activation observed around
the time of foot contact in a plyometric jump, except to say that 'this inhibition
is believed to function primarily pre-synaptically' (p. 705).
Plyometric training results in a reduction in the inhibition of muscle activity
observed around the time of foot contact (Schmidtbleicher et al., 1988), but
evidence that the reduction in inhibition is due to GTO reflex function adaptation
has not been produced. Interestingly, extensive studies by Komi of the stretch-
shortening cycle (SSC), as it is utilised in a plyometric movement, have
demonstrated reflex involvement in both the SSC and in the decrease in SSC
performance that occurs with SSC fatigue (Komi, 2000). However, the reflex
systems involved are not related to the GTO system. The short-latency muscle
spindle stretch-reflex, and receptors activating type III and IV sensory nerve
endings have been found to play a role in the SSC and its fatigue.

Other Data
Neural inhibition, preventing maximal muscle activation, has been used to
explain an unexpected deficit in maximum voluntary eccentric and slow con-
centric quadriceps force production in untrained human subjects (Aagaard et
al., 2000; Spurway et al., 2000). Following strength training, this inhibition is
reduced, allowing for more complete muscle activation and greater force
production (Aagaard et al., 2000; Spurway et al., 2000). The mechanism of the
neural inhibition, and its subsequent reduction with strength training, has not
been established(Aagaard et al., 2000; Spurway et al., 2000). Aagaard and co-
workers stated that quadriceps motoneuron activation level depends on the net
result of multiple excitatory and inhibitory inputs to the motoneuron, coming
from higher brain centres, as well as sensory pathways from muscle spindles,
GTOs, and other structures such as the anterior cruciate ligament (ACL)
 DO GOLGI TENDON ORGANS REALLY INHIBIT MUSCLE ACTIVITY 247

(Aagaard et al., 2000). Believing that their data eliminated the possibility of
the ACL input as the source of inhibition, they hypothesised that autogenic
inhibition from the GTO was the likely cause of the neural inhibition that exists
in untrained subjects and is reduced with training. However, there was no
experimental evidence to support this choice, and the role of brain centres and
other sensory systems was not addressed further.
Hutton and Atwater (1992) reviewed chronic adaptations of muscle proprio-
ceptors in response to increased use, and stated that there were no data available
on the topic of chronic adaptation of GTOs to increased use. The authors drew
attention to the common belief that, as a consequence of overload training,
GTOs become less sensitive due to a build-up of connective tissue, resulting in
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less inhibition to motoneurons. However, Hutton and Atwater indicated that this
view originated from a 1965 conference proceedings in which no experimental
evidence was presented. Thus, this view remains speculative.

SUMMARY

Part 2 of this review demonstrates that while it is commonly stated that GTO
reflex function may or does adapt following strength training, to aid in the
production of higher forces, this idea is speculative and there is no supporting
experimental evidence.

CONCLUSIONS
It would be ideal if all knowledge and recommendations in the human exercise
science literature were based on information that included experimental evidence
gathered under conditions of realistic, voluntary movement performed by humans.
Unfortunately, neurophysiological research is only rarely possible in intact
humans (or other species) performing natural movements. Accordingly, when
information is obtained under non-intact, non-voluntary conditions, care must
be taken to consider and state the limitations when extrapolating the findings
to natural voluntary movements in humans.

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