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Spinal reflex adaptation in dancers: changes with body orientation and role of pre-synaptic inhibition.

Acquisition of dance skills relies on nervous system adaptations in a variety of regions, including the spinal cord. For instance, ballet dancers have been shown to have smaller than normal muscle stretch reflexes, (1) which could be a specific neural adaptation to maintain correct positions and perform various movements required for dance. That is, depressed spinal stretch reflex responses may be a required adaptation if dancers are to reach high levels of skill development. (2)

Several studies have demonstrated that spinal stretch reflexes are modified by physical activity. (1,3,4) Important sensory information from muscles, including muscle length and the rate of change in muscle length, provides necessary proprioceptive information to the CNS. This stretch information is relayed to the alpha-motoneuron and its corresponding muscle by the spinal stretch reflex circuit, a simple one-synapse structure that can be easily studied in humans. Formation of dance-specific adaptations in the spinal stretch reflex could be dependent on the training practices used by dance educators and students.

The purpose of this article is to review the spinal stretch reflex, as well as literature demonstrating differences between dancers and untrained subjects. Data are presented on spinal reflex modulation in response to changes in body orientation, as demonstrated in differences between modern dancers and untrained subjects. Finally, the role of pre-synaptic inhibition in mediating these changes is discussed.

Neural Anatomy of the Spinal Stretch Reflex Circuit

The CNS receives information about muscle length and changes in length from specialized sensory receptors called muscle spindles located within the muscle. These are mechanoreceptors that are sensitive to stretch, and therefore detect changes in muscle length. Wrapped around the muscle spindle is the large sensory Ia afferent axon that travels to the spinal cord. When muscle stretch activates the muscle spindles information about muscle length can be sent to the spinal cord via the sensory Ia afferent axon. (5)

Sensory Ia axons make direct, monosynaptic connections to alphamotoneurons located in the ventral spinal cord. The axons of these neurons exit the spinal cord through the ventral root. The alpha-motoneuron axons connect to skeletal muscle fibers from which the spindle's sensory Ia axons arise. With sufficient input to the motoneuron cell body, an electrical signal will be sent from the spinal cord to the neuromuscular junction (the synapse between the alphamotoneuron and the muscle), creating a contraction in the stretched muscle (Fig. 1). (6) This circuit is responsible for transmitting muscle stretch information that can lead to a corrective contraction in the stretched muscle. The spinal stretch reflex circuit provides the CNS with a method for monitoring irregularities in movement trajectories across a range of muscle lengths and forces, (7) which allows for movement correction and assists in injury prevention. (8) Information from muscle spindle sensory receptors could contribute to the stability of the body when large or fast perturbations impact postural stability. For instance, if a dancer is balanced in passe and a large perturbation occurs which sends the dancer off/ balance in one direction, the opposing muscles will be stretched and the resulting reflex contraction in the stretched muscles could help return the dance to the desired position.

[FIGURE 1 OMITTED]

The alpha-motoneurons in this circuit and their connections to the muscle represent the final common assembly point for all neuromuscular communication. Alpha-motoneurons receive information from sensory receptors, such as the muscle spindle, and movement information from the brain. All movement information, regardless of where in the CNS it is processed, must pass though the spinal cord and be integrated at the alpha-motoneurons before the movement can be executed. (9) It is at this point, in the CNS, that the continual update of sensory information from the muscle spindle is combined with the voluntary commands generated by higher brain centers to produce desired movement outcomes.

Hoffmann (or H) Reflex

One way to study the monosynaptic spinal stretch reflex is through use of Hoffmann (H) reflex methodology. The H-reflex was first described by Paul Hoffmann in 1910, (10) and has been used extensively as a technique for studying sensorimotor integration and spinal cord adaptations accompanying acquisition and maintenance of motor skills. (11-13) The H-reflex is considered the electrical analog to the spinal stretch reflex, but has an important difference in that it bypasses the muscle spindle and thus facilitates study of the central mechanisms involved in motoneuron excitability, without the influence of the muscle spindle sensory receptor. The muscle spindle is bypassed because artificial electrical stimulation is applied at the sensory Ia afferent axons, rather than stretching the muscle to activate the muscle spindle.

The H-reflex is induced by electrical stimulation of a mixed peripheral nerve which contains both sensory (afferent) and motor (efferent) fibers, such as the tibial nerve, which innervates the soleus and gastrocnemius muscles (important muscles for the execution of many dance movements, as they act to plantar flex the foot). The electrical stimulus activates the large sensory Ia afferent fibers that travel to the spinal cord and synapse directly onto alpha-motoneurons. (14) With enough input the alpha-motoneurons will produce an action potential that travels along the motor efferent fibers until it reaches the neuromuscular junction. Activation of the neuromuscular junction will produce a synchronized contraction in the homonymous (target) muscle. (15,16) The synchronized contraction produces an electromyographic (EMG) response, which is recorded from surface electrodes. The most common muscle used for testing the H-reflex is the soleus muscle innervated by the tibial nerve, although other muscles have also been examined. (15)

H-reflex and M Wave

When applying low levels of electrical simulation to a mixed peripheral nerve, action potentials will first be elicited in the large diameter Ia afferent sensory axons and not in the efferent motor axons. This threshold difference is due to the fact that the Ia afferent sensory axons are larger in diameter and, therefore, have a lower threshold than the efferent motor axons. As the stimulus intensity is increased, a direct motor response called a muscle response, or M wave, will also be elicited. The M wave is the result of stimulation of the motor efferent axons that travel directly from the site of stimulation to the neuromuscular junction, without entering the spinal cord, to produce a muscle contraction. Eliciting an M wave requires higher levels of electrical stimulation than the H-reflex, because the motor axons are of smaller size and have a higher threshold. After the stimulus the M wave also occurs before the H wave, due to the shorter pathway of the M wave when compared with the H-reflex circuit (Fig. 2A).

[FIGURE 2 OMITTED]

The H-reflex can be produced both with and without an M wave. At low levels of electrical stimulation, the H-reflex will appear without an M wave due to activation of the Ia afferent axon but not the alpha motoneruon efferent axon, therefore eliciting the reflex but not the direct muscle response. (17) The H-reflex will gradually increase in size as the stimulus intensity is increased, until the H wave reaches a maximum value, called [H.sub.max]. The [H.sub.max] value represents the maximum number of alpha-motoneurons that can be activated by sensory afferent electrical stimulation, based on the given conditions. (18) The H-reflex will then gradually begin to decrease as the stimulus intensity continues to increase, and will eventually disappear from the EMG recording. With moderate to high levels of electrical stimulation to the mixed nerve, an M wave will begin to appear on the EMG recording. As stimulus intensity increases, the M wave size will also increase until all the motor efferent axons are activated. The M wave size will then plateau and remain at a maximal level, [M.sub.max], regardless of increases in stimulus intensity. [M.sub.max] is considered to represent the activation of the entire motoneuron pool, and should remain a stable number. (19) The measurement of [H.sub.max] and [M.sub.max] across a range of stimulus intensities is called a recruitment curve (Fig. 2B).

One measurement that is often used to quantify the H-reflex is the max ratio, which represents the proportion of alpha motoneurons that can be activated reflexively versus directly stimulated ([M.sub.max]). Modulation in the [H.sub.max]/M max ratio could represent changes in spinal mechanisms involved in sensori-motor integration. [H.sub.max] will be affected by spinal processes as the reflex must pass through the cord, but [M.sub.max] is not influenced by these processes as the efferent fibers do not propagate to the spinal cord. Hence, for example, increased activity of spinal inhibitory interneurons could reduce [H.sub.max], leading to smaller [H.sub.max]/[M.sub.max] ratios.

Some studies have shown dancers to have smaller [H.sub.max]/[M.sub.max] ratios compared to both athletes and untrained subjects. (1) Modulation in the [H.sub.max]/M max ratio has been suggested to be a training-induced adaptation in dancers. Decreases in the [H.sub.max]/[M.sub.max], as seen in dancers, could be the result of a spinal adaption to control the flow of incoming sensory information to the motoneuron and thus to the muscle force production. Control over incoming sensory information may be one method dancers use to achieve expert levels of muscular control. For instance, decreasing the sensory input from the Ia axons onto the alphamotoneurons could allow cortical areas to maintain greater control over alpha-motoneuron output. Increased cortical control could increase movement precision.

The Influence of Interneurons on the H-reflex

Although the spinal stretch reflex circuit is monosynaptic, it is subject to the influence of both spinal interneurons and pre-synatpic inhibition. Interneurons and pre-synaptic inhibition both have powerful modulatory effects on the spinal stretch reflex circuit and may in fact be the locus of the observed reflex differences in athletes trained for different activities. (20) Interneurons are the most abundant neurons in the CNS, and they influence the excitability of the alphamotoneurons. (21) Interneurons in the spinal cord serve a variety of functions, including 1. relaying sensory inputs to modulate the output of motoneurons, and 2. relaying and modifying descending supraspinal inputs to the motoneurons. (22) Interneurons integrate information and transmit it to the alpha-motoneurons, impacting motoneuron output to the muscle.

One interneuronal mechanism that has shown modulation in dancers is reciprocal Ia inhibition. Reciprocal Ia inhibition involves Ia sensory afferents from the muscle spindle. The Ia afferent axons branch within the spinal cord to synapse not only on the alphamotoneurons, but also on inhibitory interneurons that synapse onto the alpha-motoneurons antagonistic to the muscles from which their Ia input originates. Reciprocal inhibition allows for coordinated contraction of opposing muscles in which the agonist contracts as the antagonist relaxes. Professional ballet dancers have shown decreased levels of reciprocal inhibition compared to other athletes when the soleus muscle is tested. (1) These decreases could be attributed to daily training of co-contraction in dance class. The reduction in dancers' level of reciprocal inhibition could be the result of needed co-contraction of antagonistic muscles in the lower leg (1,23) to maintain balance for dance positions, such as arabesque.

[FIGURE 3 OMITTED]

The Influence of Pre-synaptic Inhibition on the H-reflex

Sensory information from Ia afferents is constantly flowing to alpha-motoneurons, resulting in an overwhelming input to the spinal cord. In order to properly control complex motor tasks, such as dance, this sensory information must be restrained to avoid unwanted oscillatory movements (such as tremor or postural sway). One method used by the nervous system to modulate sensory inflow of information from Ia afferents is pre-synaptic inhibition. (24) Pre-synaptic inhibition acts by modulating transmitter release from the Ia afferents to the alpha-motoneuron (Fig. 3). Modifying incoming sensory input to spinal alpha-motorneurons is an important part of adjusting the amount of influence Ia sensory afferents have on the alpha-motoneurons when performing movements. (24) Decreases in the amount of sensory input from the spinal stretch reflex might allow supraspinal centers, such as the cortex, to maintain greater levels of control over the working muscles. Increases in pre-synaptic inhibition (along with decreases in reciprocal Ia inhibition) have been associated with the ability to maintain co-contraction in antagonistic muscles of the lower leg (25) and learn complex motor skills. (13) Differences in pre-synaptic inhibition have been demonstrated between athletes trained in various sports. (26) It is possible that the smaller [H.sub.max]/ [M.sub.max] ratios observed in dancers could be partially explained by increases in pre-synaptic inhibition.

Although previous studies have demonstrated neuro-plasticity with dance training, to date no studies have examined the role of specific presynaptic mechanisms in modulating spinal reflexes in dancers. Pre-synaptic inhibition is a proposed mechanism that might be responsible for part of the neuro-plasticy seen in dancers. (1,4) The purpose of this study was to examine the influence of pre-synaptic inhibition on reflex profiles in trained modern dancers. Pre-synaptic inhibition was examined by comparing H-reflexes in dancers with those in untrained subjects, in both standing (weight bearing) and prone (nonweight bearing) body positions.

Methods

Subjects

Ten subjects, aged 22 [+ or -] 14 years, participated in this study (7 women, 3 men). Five of the subjects were college students with a minimum of 10 years of dance training seeking a degree in modern dance at Indiana University. The other five subjects were nonathlete controls with no prior dance training. All were apparently healthy, with no history of neuromuscular deficits, as based on a questionnaire. They gave their informed consent to the experimental protocol, which was approved by the university's Committee for the Protection of Human Subjects.

Procedures

Soleus H-reflex recruitment curves were measured for all subjects. Recruitment data were collected under four conditions: in both standing and prone positions, with either presynaptic inhibition conditioning or no conditioning. The entire recruitment curve was measured four times, under all conditions, for each subject. Surface electrodes (Ag-AgCl) with 2 cm intra-electrode distance were used for recording electrical muscle activity (EMG). EMG activity was recorded from both the tibialis anterior muscle and the soleus muscle of the subject's right leg. Two surface stimulating electrodes were used to elicit the soleus H-reflex: a cathode electrode (0.8 cm diameter) was placed on the popliteal fossa (behind the knee), and an anode electrode (4 cm diameter) was placed just superior to the patella (knee cap).

In half the trials simple unconditioned H-reflexes were measured. Soleus H-reflexes were elicited by tibial nerve stimulation with a 1 millisecond duration pulse, using standard H-reflex measurement procedures. (27) These reflexes were elicited every 10 seconds, with gradually increasing stimulus intensity. In the other half of the trials stimulation of the common peroneal nerve (CPN) was added, 100 ms prior to the soleus Hreflex stimulus, to assess pre-synaptic inhibition. The CPN innervates the anterior and lateral muscles of the lower leg, which are antagonistic to the soleus muscle. CPN stimulation activates Ia afferent axons from the anterior lower leg muscles that project to spinal inhibitory interneurons. The spinal inhibitory interneurons project to the Ia afferent axons arising from the soleus muscle and inhibit chemical neuro-transmitter release from the soleus Ia afferent axons to the alpha-motoneurons. CPN conditioning (Fig. 4) of the soleus H-reflex is a commonly used method for assessing pre-synaptic inhibition (27) and provides an assessment of the communication between an antagonist and agonist muscle group of the ankle joint. CPN stimulation was induced by placing a cathode electrode on the right leg just distal to the fibular head and an anode electrode on the medial aspect of the knee (Fig. 5). The stimulus intensity for the CPN conditioning was set to 1.5x motor (M wave) threshold for the tibialis anterior muscle.

[FIGURE 4 OMITTED]

[FIGURE 5 OMITTED]

Experimental Protocol

For each subject H-reflex recruitment curves were tested in four different conditions: 1. prone with no CPN conditioning; 2. prone with CPN conditioning; 3. standing with no CPN conditioning; and 4. standing with CPN conditioning. Subjects started in either the standing or prone position, assigned randomly. Soleus H-reflex recruitment curves with no CPN conditioning were tested first in each body position.

Data Analysis

EMG signals from the soleus muscle were stored on a computer for off-line analysis using the AcqKnowledge System data collection software (Biopac Systems, Goleta, CA, USA), with a sampling rate of 2 kHz per channel. A band-pass Butterworth filter (20Hz450Hz) was applied to all EMG signals. Amplitude (peak to peak) of the raw H-reflex or M-wave created by each stimulus was measured, followed by determination of [H.sub.max] and [M.sub.max] values for each subject. The dependent variables were the [H.sub.max]/[M.sub.max] ratios, unconditioned and with CPN conditioning, which were expressed as percent values. A three-way ANOVA (subject group by posture by conditioning) with repeated measures for posture and conditioning was applied for statistical analyses, and the level of significance was set at 0.05.

Results

Dancers had significantly [[F.sub.(1,8)] = 6.99, p = .030, [[alpha].sup.2] = 0.24] lower [H.sub.max]/ [M.sub.max] ratios (mean = 27.29%) compared to control subjects (52.12%), regardless of posture or conditioning (Fig. 6). A significant reduction of 6.73% [[F.sub.(1,8)] = 10.21, p = .013, a2 = 0.34] in the [H.sub.max]/M max ratio also occurred during standing compared to prone across all subjects. A significant interaction occurred between posture and conditioning [F(u6) = 20.47, p = .002, [[alpha].sup.2] = 0.37] in which CPN conditioning only induced significant reductions of 28.86% in the [H.sub.max]/ [M.sub.max] ratio in the prone posture across all subjects (Fig. 7).

Discussion

The results of this study are in agreement with those from previous studies, (1,3,4) that dancers have lower so leus H max/[M.sub.max] ratio s when compared to untrained subjects. To the best of our knowledge this is the first H-reflex study to provide evidence of soleus H-reflex depression in modern dancers; previous studies on dancers have examined H-reflex depression in ballet dancers. Lower soleus [H.sub.max]/[M.sub.max] ratios suggest that the motor skill training for dance involves plasticity (adaptation) of specific spinal mechanisms. One of the initial H-reflex studies on dancers was performed by Mynark and Koceja (4) in 1997. These authors examined the difference in soleus H-reflex gain (the ratio between the amplitude of the H-reflex, measured at 50% of [H.sub.max], and the background EMG) between dancers and untrained subjects. Gain was measured in both standing and prone postures at rest, and at 10%, 20%, and 30% of maximal voluntary soleus contraction. The results indicated that both dancers and untrained subjects suppressed the [H.sub.max]/M max ratio when changing body orientation from prone to standing. Interestingly, the results also demonstrated that while dancers and control subjects displayed similar reflex gain in the prone position, dancers had significantly lower reflex gain in the standing position. The results of the Mynark and Koceja study suggest that dancers modulate spinal reflexes differently than control subjects in the standing posture. Suppression of incoming sensory input from the Ia axons has been suggested by Nielsen1 to be important for postural control in dance, because reflex information transmitted by the sensory Ia fiber could interfere with dynamic balance, and hyperactive reflex circuits may produce unwanted body oscillations when maintaining a static dance position such as a balance on releve. The exact spinal mechanism responsible for reflex plasticity in dancers is presently not well understood.

[FIGURE 6 OMITTED]

[FIGURE 7 OMITTED]

The current study examines one inhibitory mechanism, pre-synaptic inhibition, that has been suggested to be responsible for the H-reflex depression seen in dancers. Both dancers and control subjects demonstrate reflex suppression when standing; however, pre-synaptic inhibition, elicited by CPN conditioning to the soleus H-reflex, was not different between dancers and untrained subjects. Although dancers had lower [H.sub.max]/M max ratios compared to untrained subjects, they did not appear to modulate the H-reflex differently from untrained subjects between standing and prone postures.

Based on the data collected it is not possible to tell which spinal mechanism results in the decreased H-reflex seen in dancers, but it is safe to conclude that these differences are not solely governed by pre-synaptic inhibition from the antagonist musculature. It is possible that other spinal mechanisms, such as recurrent inhibition and/or reciprocal inhibition, are responsible for the depression of the H-reflex seen in dancers.

It is also possible that protocols for assessing pre-synaptic inhibition other than CPN conditioning could explain the difference in [H.sub.max]/[M.sub.max] ratios seen between dancers and control subjects. For instance, another method of assessing pre-synaptic inhibition involves femoral nerve stimulation to examine the relationship between the quadriceps muscle and the soleus muscle. Femoral nerve stimulation is a significantly different form of pre-synaptic measurement than the CPN conditioning protocol. Femoral nerve conditioning measures the ongoing tonic level of pre-synaptic inhibition from the quadriceps muscle reaching Ia sensory axons of the soleus muscle. (19) CPN conditioning, on the other hand, assesses the effects of activation of pre-synaptic inhibition from the antagonistic muscle (tibialis anterior) on the soleus alpha-motoneurons. (27) A wide variety of H-reflex conditioning protocols exist to examine specific spinal mechanisms, and more studies will be needed to discover the specific mechanisms involved in reflex suppression in dancers.

Relevance to Dance Medicine and Science

To have an informed basis for dance training requires an understanding of the extent to which the CNS can adapt to training before long-term changes in behavior occur. Adaptive plasticity in the human spinal cord is associated with the acquisition and mastery of motor skills, such as dance. Changes in the spinal stretch reflex circuit could be a necessary part of motor skill learning for dance. Previous studies have demonstrated spinal adaptations with dance training, including differences in the soleus H-reflex between dancers and control subjects. Spinal adaptations might account for some of dancers' enhanced balance and ability to perform complex motor tasks. Understanding how specific dance training practices effectively develop the neuromuscular adaptations necessary for high level performance would be of great benefit to both dance educators and students. For example, mental imagery training has been shown to modulate H-reflex amplitude. (28) It is possible that mental imagery training could be a beneficial technique for assisting in the creation of the neuromuscular adaptations needed for refinement of dance skills, such as balance and movement precision.

The relationship between reflex plasticity and elite dance performance is not straightforward, and more research is needed to explore further how modulation of specific spinal mechanisms results in enhanced performance. Future research that focuses on how different training techniques (mental imagery, strength training, various dance genres) influence spinal reflexes in dancers could provide valuable insights into how dancers develop their refined motor skills. The use of H-reflex methodology provides a way to study spinal adaptations in dancers such as changes in [H.sub.max]/[M.sub.max] ratio, reciprocal inhibition, and presynaptic inhibition.

Conclusion

It was concluded from the data analysis that: 1. modern dancers have smaller [H.sub.max]/[M.sub.max] ratios than control subjects; 2. the [H.sub.max]/[M.sub.max] ratio is smaller in standing than in prone among both dancers and controls, indicating that the CNS may suppress reflex input to increase postural stability; and 3. pre-synaptic inhibition is not different between modern dancers and controls in standing, indicating that both groups modulate their stretch reflex input in similar ways. The small sample size used in this study resulted in low statistical power. Only modern dancers were used in this study. It is possible that pre-synaptic inhibition, elicited by CPN conditioning to the soleus Hreflex, might be an important spinal mechanism used in ballet and other forms of dance. Other spinal mechanisms may be involved in producing the smaller reflexes seen in modern dancers. Dance specific studies, using H-reflex methodology, could increase our understanding of the specific spinal cord mechanisms involved in the acquisition and maintenance of dance skills.

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Rachel Ryder, M.S., Koichi Kitano, M.S., and David M. Koceja, Ph.D.

Rachel Ryder, M.S., Koichi Kitano, M.S., and David M. Koceja, Ph.D., are in the Motor Control Laboratory, Department of Kinesiology and Program in Neuroscience, Indiana University, Bloomington, Indiana.

Correspondence: Rachel Ryder, M.S., Department of Kinesiology and Program in Neuroscience, Indiana University, HPER 121, Bloomington, Indiana 47405; rabritto@indiana.edu.
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Title Annotation:Original Article
Author:Ryder, Rachel; Kitano, Koichi; Koceja, David M.
Publication:Journal of Dance Medicine & Science
Article Type:Report
Geographic Code:1USA
Date:Oct 1, 2010
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