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Proprioception: The Forgotten
Sixth Sense
Chapter: Respiration and Proprioception
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I
eBooks
Respiration and Proprioception
Ufuk Yurdalan S1* and Ilksan Demirbuken2
Professor, Marmara University, Health Sciences Faculty, Physiotherapy &
Rehabilitation Department, Istanbul, Turkey
1
Assistant Professor, Marmara University, Health Sciences Faculty, Physiotherapy &
Rehabilitation Department, Istanbul, Turkey
2
*Corresponding author: Ufuk Yurdalan S, Professor, Marmara University, Health
Sciences Faculty, Physiotherapy & Rehabilitation Department, E-5 Yan Yol Üzeri,
34865 Cevizli /Kartal - İstanbul, Turkey, Tel: 90 216 399 93 71; Fax: 90 216 399 62 42;
E-mail: ufukyurdalan@hotmail.com
Abstract
In this chapter the main concepts concerning respiration and respiration related to
proprioceptive mechanisms are introduced and discussed. The discussion of respiration
and proprioception is basically focused on the breathing work and its control through
proprioceptive properties at both neuromusculoskeletal and respiratory systems. Also this
chapter was supported by an author opinion and case study presentation. Due to lack of
‘Respiration and Proprioception’ studies in the literature, thoughts about proprioceptive
effects on respiration consist mainly of technical comments.
Keywords:
Dyspnea; Proprioception; Respiration; Respiratory Muscles
What is ‘Respiration’?
In simple terms, respiration exchanges gases by supplying oxygen to and eliminating
carbon dioxide from the lungs [1]. Respiration has two phases as inspiration and expiration.
Inspiration, breathing in, occurs as a result of negative intrapleural pressure created by
lower lung volumes. To have lower lung volumes, lateral and anteroposterior diameter of
thoracic cage should increase. Surrounding muscles and involved joints cause the changes
in diameter of thorax. Expiration is a passive process; therefore, it does not need any active
muscle contraction, except for forceful activities such as coughing or sneezing [2].
Neural Control of Respiration
Breathing or respiration is controlled by the automatic control structure which is located
in the brainstem and voluntary control structures in the cerebral cortex. The respiratory
center in the brainstem controls both the depth (volume) and rate (frequency) of breathing
via neural and chemical control. Two major groups of respiratory neurons are found in the
respiratory center. The dorsal respiratory group located dorsomedially in the medulla and
sets tidal volume. The ventral respiratory group is found ventrolaterally in the medulla.
1
They involve inspiratory and expiratory neurons whose stimulus transmits to the spinal
respiratory motor neurons for intercostal, abdominal and phrenic innervation. During
sleeping and normal breathing the automatic centers are responsible for controlling
breathing rate and volume. In case of maneuvers such as speaking, coughing, singing and
holding breath, cortical centers take over voluntary control of breathing. Outputs from
mechanoreceptors and chemoreceptors in the respiratory system stimulate or inhibit the
action of components of the respiratory centers [3].
Chest Wall Movements
During inspiration the rib cage moves up and out to increase the mediolateral and
anteroposterior diameter of the chest [1]. The expansion of the chest wall reduces the
pressure in the lungs and creates a pressure differential that allows air flow into the lungs
[3]. Oppositely, during expiration the rib cage returns to its starting position by moving
down and in to decrease the increased chest diameter. Two types of chest wall movement
have been described according to the direction of the chest wall expansion. The movement
which increases the mediolateral diameter of the rib cage has been associated with the up
and down movement of a ‘bucket handle’. The lateral aspect of the ribs moves up and away
from the vertebral column and sternum in the way that a handle moves up and away from
the bucket [1,3].
The second type of movement changes the anteroposterior diameter of the chest by
moving the ribs and the sternum in an upward and outward direction. This movement is
comparable to movement of pump and its handle so that it is called ‘pump-handle’ effect [1].
The Role of Respiratory Muscles in Chest Wall Movements
It is well known that the contributions of the inspiratory and expiratory muscles are
necessary for the proper displacement of the chest wall during breathing. The primary
muscles of inspiration are the diaphragm and intercostal muscles, especially the external
intercostal muscles. If a deep or labored inspiration is required, the accessory muscles of
inspiration are activated. By relaxing of inspiratory muscles, expiration occurs as a passive
process. During forced expiration, the abdominal and internal intercostal muscles are
recruited [3,4]. The chest wall movements which have been defined above primarily occur by
intercostal muscles and accessory muscles accompany the respiration in the time of need.
Proprioceptors in the Respiratory System
The largely responsible muscles for respiration are diaphragm, intercostals and
abdominal muscles. Many other muscles have an accessory function including muscles in
the neck and perineum [5].
Respiratory muscles have mechanoreceptors which have functions on central control
of breathing. The muscle spindle endings and tendon organs which are generally classified
as proprioceptors are considered to be the primary receptors [6]. The activity of respiratory
muscle afferents provides muscle mechanical information during respiration [7]. The results
of previous investigations indicated that these receptors were sensitive to changes in muscle
length and velocity of stretch during spontaneous breathing [7-9]. Intercostal muscle
spindle receptors have been identified into two basic types as 1˚ and 2˚ endings [10,11].
The 1˚ muscle spindles are more sensitive to the velocity of stretch while the 2˚ afferents
are sensitive to static length changes. The Golgi tendon organ which is the third type of
mechanoreceptor was also shown to be responsive to muscle contractions [12].
Afferents of 1˚ and 2˚ muscle spindle endings of intercostals have monosynaptic
connections with homonymous motoneurons of the same spinal segment [13,14]. Afferents
of 1˚ muscle spindle endings also excite homonymous motoneurons of adjacent segments
monosynaptically and distal segments polysynaptically [6,15]. On the other hand, afferents
2
of tendon organs from intercostals have an inhibitory effect on homonymous motoneurons
of the same segments [15].
Researchers have tried to distinguish functions and specific effects of different muscle
spindle endings on brainstem control of breathing by using electrical nerve stimulation
methods. The mechanisms by which respiratory muscle proprioceptors influence neurons
in respiratory centers are not clear due to major limitations of using electrical current to
stimulate nerve afferents. It is difficult to stimulate the proprioceptors or their afferents
selectively. The recruitment order for proprioceptor afferent fibers by increasing electrical
voltage has been revealed. Thus, only the 1˚ muscle spindle endings (especially group Ia) can
be selectively stimulated. The results of the studies showed that stimulation of intercostal
and abdominal muscle group 1˚ fibers prolonged duration of expiratory phases [16].
The projection pathways for proprioceptors of intercostals were found to be similar to
those of other skeletal muscles involving the thalamus, cerebellum and cerebral cortex.
The spinal circuits of the intercostal proprioceptors are complex in their structure and
have connections between their afferents and the motoneurons of homonymous intercostal
muscles and another connection with the phrenic moto-neuron pool. Previous studies
focused on the activity of proprioceptors during breathing and used chest wall distortion
to understand how their activity was affected. Some of the researchers used vibration to
activate proprioceptors of intercostals. They have shown that vibration of the intercostal
muscles, chest wall and sternum changes the respiratory pattern [17-20]. It is not clear if
muscle spindle endings were the only activated mechanoreceptor in response to vibration.
Both muscle spindle endings and tendon organs may be activated due to application of
larger vibration amplitudes [6].
The primary inspiration muscle, the diaphragm, shows a difference in proprioceptive
innervation compared to other skeletal muscles including the intercostal muscles in
terms of quantitative properties [21]. Work of Euler showed that there was a low ratio
between the muscle spindle and tendon organ afferents, which was considered to be an
important functional characteristic of diaphragm [22]. There is no evidence that diaphragm
mechanoreceptors affect brainstem respiratory neuron activity [6]. The researchers, who
performed sectioning of cervical dorsal roots and interruption of phrenic nerve afferents
from the diaphragm, indicated that the diaphragm had no influence on respiratory functions
of spontaneously breathing cats or rabbits [21]. Other studies with low-voltage electrical
stimulation of phrenic nerve afferents also showed that diaphragm proprioceptor afferents
had no significant effect on brainstem respiratory control [23].
The studies showed that the projection pathway for diaphragmatic proprioceptors was
similar to proprioceptors located in other skeletal muscles like intercostals. Collaterals of
afferent fibers ascend within the dorsal column of spinal cord and synapse in the cunate
nucleus. Second neurons cross the
midline at the medial lemniscus and project on neurons in the thalamus. Finally,
neurons from thalamus terminate to somatosensory cortex [16].
The abdominal muscles are recruited by forced expiratory effort, and therefore they are
not ordinarily active during quite breathing. It means that their proprioceptors are not likely
to affect the control of the quite breathing pattern [6].
To sum up the effects of the muscle mechanoreceptors, muscle spindle endings and
tendon organs, it can be stated that muscle proprioceptors are participated in regulation
of level and timing of the respiratory function. Muscle proprioceptors may also involve in
increasing the ventilation during the early stages of exercises. Tendon organs are sensitive
to change in force of muscle contraction and have inhibitory effect on inspiration. They may
be important in coordination of respiratory muscle contraction during breathing [24].
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As mentioned before, to make the air exchange possible muscular mechanisms are required.
When the respiratory muscles are activated, they change thoracic volume by providing
movement of joints involved in the thorax [1]. Joint mechanoreceptors are responsible for
perception of movement and its direction. It has been found that costovertebral joints in the
thoracic cage have mechanoreceptors. Unfortunately, the functions of mechanoreceptors
in costovertebral joints have not been largely studied compared to mechanoreceptors in
limb joints. Although there are a limited number of studies, it could be concluded that
costovertebral mechanoreceptors discharged with spontaneous breathing movements of
the thoracic cage. Some of these receptors are defined to be sensitive to movement in an
inspiratory direction and some of them to an expiratory direction [25]. It was speculated
that regardless of their directional sensitivity, costovertebral joint mechanoreceptors have
the same effect on respiratory pattern [6]. To conclude, joint mechanoreceptors are sensitive
to movement of chest wall and likely to influence the level and timing of the respiratory
activity. Afferents of proprioceptors affect the firing rate of phrenic motor neurons via their
projections. In addition they project to the medullary respiratory group and influence the
timing of inspiration and expiration [24,26].
Dyspnea and Proprioceptors in the Respiratory System
The sense of dyspnea, which is described as breathlessness experienced by patients,
is also thought to be related with the proprioceptors in the respiratory system. The
primary mechanism in the relation between proprioceptors and dyspnea is length-tension
inappropriateness arising from respiratory muscles [24].
It is explained by a case report history, a 74-year-old man presented with dyspnea on
minimal exertion for several weeks, the brief explanation of a case in the review of Brandon
et al., as follows:
‘A chest radiograph of the patient showed a large right pleural effusion with mediastinal
shift to the contralateral side accompanying with several physical symptoms and signs. A
1.5-L therapeutic thoracentesis was performed, with dramatic improvement in the patient’s
symptoms. The patient returned to the clinic several weeks later with recurrence of his
symptoms of shortness of breath with minimal exertion. Physical examination confirmed
re-accumulation of the pleural fluid. Right-sided pleurodesis was ultimately performed with
no pleural fluid recurrence and excellent long-term relief of his dyspnea. This patient had
dyspnea primarily resulting from the presence of a large pleural effusion. This appears to
arise primarily by the mechanism of length-tension inappropriateness caused by a pleural
effusion stretching the chest wall. According to this hypothesis, inspiratory muscle activation
produces muscle contraction and a degree of tension in the muscles that is sensed by the
tendon organs. If the respiratory muscles are inefficient for mechanical reasons (in this
case because of the thoracic distention produced by the pleural effusion), the magnitude of
tension in the muscle produced by a given amount of muscle contraction is proportionately
lower than in the normal state. This discrepancy between the degree of neural input to and
contraction of the respiratory muscles and the tension produced by that muscle contraction
is sensed by the cerebral cortex as dyspnea. Removal of the pleural fluid in this case had
the effect of reducing end-expiratory muscle fiber length and restoring the relationship of
muscle contraction and muscle tension to normal, thereby immediately reducing dyspnea’
[24,27].
Posture and Respiration
The posture of a person affects his or her lung volume, ventilation, compliance, gas
exchange, mucociliary clearance and muscle work [28]. Besides their ventilator function,
respiratory muscles also have an important function in postural alignment and alterations
in posture can also influence the respiratory functions of these muscles [29,30]. It is quite
likely associated with alterations in mechanical efficiency due to length-tension changes.
4
The influenced respiratory functions are expected as a result of changes in joint orientation
and muscle activity via altered compliance of both the abdominal and thoracic regions
caused by length-tension changes. Furthermore it is demonstrated that even single plane
changes in sitting posture altered three-dimensional ribcage configuration and chest wall
kinematics during breathing by study of Joe Lee et al., [30].
Furthermore the major respiratory muscle, diaphragm, was found to be contracted
during functional tasks. It is active with a rapid movement of contralateral upper extremity,
especially movement of shoulder and elbow, not with wrist and digits [29]. It can be speculated
that diaphragm is also recruited by tonic and phasic movement related commands [31].
Proprioception is a primary sense for postural balance; therefore, proprioceptive inputs from
respiratory system can be related with balance control. Diaphragm has an important role
in stabilizing the trunk during activities requiring balance [32]. The study which included
individuals with chronic obstructive pulmonary disease identified impaired postural balance
by indicating poor proprioceptive control in these patients compared to healthy controls.
Briefly, their results suggested that respiratory muscle weakness contributes to impaired
proprioceptive postural control [33]. It might happen due to increased respiratory loading of
diaphragm; therefore, it could not contribute to trunk stabilization and switch its function
on postural balance into respiration [32].
Interventions Used by
Respiratory Functions
Physiotherapists
to
Improve
There are several approaches used by physiotherapist for management of the patients
with respiratory problems. The main purpose of these physiotherapy techniques is to
improve respiratory functions by encouraging maximal inspiration, increasing strength and
endurance of respiratory muscles, increasing inspiratory volume and clearing secretions
from the system.
Here some of the treatment approaches and its relations with the proprioceptors in the
respiratory system are summarized.
Proprioceptive neuromuscular facilitation technique for enhancing respiration
Proprioceptive Neuromuscular Facilitation (PNF) technique is defined as a concept of
treatment which is a positive functional approach to help patients achieve their highest level
of function. It has been shown to improve muscle functions and range of motion of joints by
various studies [34]. Breathing problems can be resulted from both disturbed inspiration
and expiration phases. To enhance breathing the related structures involving diaphragmatic,
sternal and costal areas are treated. Facilitations of chest, trunk and shoulder mobility are
the other treatment approaches. The physiological mechanism that facilitates the initiation
of inspiration is thought to be the stretch reflex. The stretch reflex resists the change in
muscle length by contracting to stretched muscle via its muscle spindle (proprioceptor).
Generally, PNF technique continues with repeated stretch through range to facilitate an
increase in inspiratory volume. Appropriate resistance during applying one of the PNF
techniques strengthens the muscles and guides the chest motion [35].
Breathing exercises and respiratory muscle training
Breathing exercises aim to improve basal, lateral and apical chest wall expansion and
diaphragmatic excursion [2]. Based on the previous knowledge it can be assumed that
movement of the chest wall stimulates the mechanoreceptors in the thorax especially muscle
spindle endings which are primarily influenced by changes in length of muscle.
The primary purpose of respiratory muscle training is to improve respiratory muscle
strength and endurance. It has been well documented that increased muscle strength and
endurance gained by this training has a positive effect on symptoms, exercise capacity and
5
health-related quality of life outcomes of patients suffering from respiratory problems [36].
Given these knowledge so far, we can speculate that respiratory muscle training should
have impact on mechanoreceptors of the respiratory muscles. Austin et al., indicated that
proprioceptive muscular education via Alexander technique enhanced ease of breathing.
Individuals improved their body awareness and learned the efficient breathing pattern by
voluntary inhibition of personal habitual patterns of rigid musculoskeletal structure [37].
A recent study of Janssens et al., revealed a relation between breathing exercises and
proprioceptive use of peripheral muscles which are involved in the maintenance of postural
balance. They included the individuals with low back pain in their study who have greater
tendency to diaphragm fatigue. Study and control group were trained by high and low
intensity inspiratory muscle training. After 8 week of training they indicated that back
proprioceptive use improved by discouraging the trunk stabilization function of diaphragm.
This improvement is thought to be achieved by modifying pain gate control [38].
Further studies are required to investigate this topic on proprioceptors and respiratory
muscle training.
Incentive spirometer
Incentive spirometer is widely used device in physiotherapy settings especially after
surgery to maintain clearance of respiratory system and inhaled lung volume. The pattern
of breathing while using incentive spirometer is important. It promotes deep inhalation and
slow breathing patterns [39]. As previously discussed for other physiotherapy techniques
used by physiotherapist such as respiratory muscle training and breathing exercises
we could just make estimations on relation between incentive spirometer training and
activation of proprioceptors involved in respiratory system. Incentive spirometer should play
a role in recruitment of mechanoreceptors of chest wall and muscles due to chest expansion
occurred by deep inhalation.
Acknowledgement
Authors cordially thank to Assoc. Prof. Arzu Arı, PhD, RRT, PT, CPFT, FAARC for scientific
and clinical support under the title.
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