Proprioceptive system

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Introduction[edit]

Body movement is an essential component of human life. In everyday activities, or competitive sports, the generation of precise and coordinated movement is essential to interact with the environment. This depends on signals coming from the body that allows it to respond to its surroundings and to react to changing circumstances [1] [2]. Besides the usual senses that are responsible for our interaction with the external world (sight, sound, smell, touch, and taste), there are other ones responsible for our internal functioning. The knowledge about position and movement of the limbs and trunk is provided by sensations arising in proprioceptors. This allows a person to maneuver around obstacles in the dark, or to manipulate objects out of view, for example. This internal sense, often referred to as the sixth sense, is called proprioception. It affects our lives continually, allowing the accomplishment of complex tasks that would be impossible without it. As an example to show the impact of the absence of proprioception, moving a finger would be extremely difficult. Without proprioception the brain cannot feel what the finger is doing, and the process of moving it would have to be carried in a more conscious and calculated way, compensating the loss of positional feedback with vision. Another example that shows the relevance of proprioception is driving. Drivers are able to keep their eyes on the road while adjusting their arms and hands on the wheel, and applying the correct amount of pressure to the pedals [1] [3] [4].

Proprioception is not bounded by visual cues. Even when vision is absent, there is a correct sense of limb position. At any time, a person still knows the position of the different body parts during a movement and has an accurate map of their position in space. Therefore, the proprioceptive system allows precise placements such as touching the tip of the nose with the eyes closed [5].

Perception “is the identification, organization, and interpretation of sensory information, in order for humans to internally represent and understand the environment [1].” Perceptions need signals within the nervous system. These derive from physical stimulation of the various sense organs. In the same way, proprioception requires the stimulation of mechanoreceptors via changes of body position. Specifically, proprioception pertains to the perception of body position and movements in a 3D space. The peripheral mechanoreceptors provide proprioceptive information to the brain, in order for it to integrate and use them. The physical receptors (e.g. skin, muscles, or joints) can be seen as the hardware component, and the central processing that analyses the signals, the software [1] [4] [6] (1; 4; 6).

Recently, it was demonstrated that proprioception as a measure of neuromuscular response to a stimulus must involve sensory input, central processing, and motor output. Therefore, proprioception cannot be interpreted has only the afferent (hardware) part of the system, the cumulative neural input to the nervous system from the receptors located in muscles, joints and the skin. Although muscles spindles are considered the main receptors of proprioceptive information, there is a complex array of different sources and the importance of central processing in proprioception has been increasing in recent years [1].

A deficit in proprioception will lead to a loss of controlled movements without continuous visual feedback, a severe difficulty in maintaining force or position, and tremors could develop. It is an essential sense for the coordination of movement [5].

According to Proske et al. (2012), “the subject of proprioception lies at the boundary between neurophysiology and neuropsychology.” It can be considered a mysterious sense since we are largely unaware of it. In the absence of vision, the limbs positions is still known but there is no clearly defined sensation that can be identifiable. This can be explained by the predictability of proprioceptive signals. There is an awareness that a person is making a willed movement and so the sensory input that it generates is anticipated. In sensory physiology there is a concept that what we feel commonly represents the difference between what is expected and what actually occurs. Regarding proprioception, if there is no mismatch between the expected signals from a movement and those generated, there is no definable sensation, but the person still knows the location of their limbs precisely [5] [7].

Besides the proprioceptive system, the vestibular system contributes to several conscious sensations as well as helping with movement and posture. Conscious sensations include the senses of limb position and movement, the sense of tension or force, the sense of effort, and the sense of balance. Kinaesthesia is a term that can be used to refer to sensations of limb position and movement. Conventionally, proprioception consists of four senses that consist of the conscious sensations described before, and it is the cumulative neural input to the central nervous system from various receptors that collect sensory information from the body [2].

The control of a movement is dependent on the quality of the afferent input originated from the various somatosensory systems, like the interoceptors (for the detection of a stimulus within the body) and mechanoreceptors (specialized nerve endings) that are involved in proprioception. These mechanoreceptors can be located in the joints, capsules, ligaments, muscles, tendons and skin [2].

Traditionally, muscle spindles have been responsible for providing the primary signals that contribute for the sense of limb position. There are several studies that used muscle tendon vibration manipulation (which stimulates preferentially muscle spindles afferent) that have produced illusions of joint position and motion. Recently, the sense of effort has been gaining ground regarding its role in joint position sense. Finally, as mentioned, beyond the peripheral aspects of proprioception, there is a significant central component to sensing body positions and movements. This was discovered through studies in the 1970s that assessed “the accuracy of reaching to proprioceptive targets that were either established through active movement of the subject or passive displacement by the experimenter” [2] [8].

Proprioception and kinaesthesis[edit]

Both “proprioception” and “kinaesthesis” are terms that continue to be used in the scientific literature, sometimes with different interpretations according to the authors. Some researchers define proprioception as the sense of joint position only, while kinaesthesia as the conscious awareness of joint motion. Others consider kinaesthesia as one of the submodalities of proprioception. In this case, proprioception contains both joint position sense and the sensation of joint movement. This last definition is in accordance with the conceptualization of kinaesthesis that was originally coined by Bastian (1888): the ability to sense the position and movement of limbs and trunk. Dover and Powers (2003) include the joint position sense, kinaesthesia, and sense of tension or force as submodalities of proprioception. It has also been argued that “proprioception” and “kinaesthesis” can be synonymous [1] [5] [7] [9] [10] [11].

The study of proprioception[edit]

Like any other field of knowledge, the study of proprioception has been evolving. This area has, traditionally, attracted vast interest due to the role played by proprioception in motor control. Besides this, a greater knowledge of the mechanisms of proprioception promises a better understanding of the human sensory experiences. Developments in neuroimaging, like magnetic resonance imaging (MRI), has allowed the study of the central activity patterns produced by proprioceptive inputs. This is leading to advancements in the understanding of how some proprioceptive sensations arise and how they are used to create a body image. Besides this, there is a field of study concerned with the interactions between proprioception, vision, and vestibular inputs [2].

Studies that observed motor cortical neurons concluded that the brain is not concerned with information about muscle length changes from individual afferents, but with the population of muscles afferent input signals that arises in groups of muscles. Another area that has been explored is the relation between proprioception and fatigue from exercise. Some of the clumsiness in movements felt after intense exercise could have an origin in proprioception. An important point is age and proprioception. Evidence shows that a decline in proprioception due to age is responsible for an increase in falls in the elderly [2].

Brief historical background[edit]

There have been speculations about a muscle sense that date back at least to the 17th century. Von Helmholtz proposed the theory of “sensation of innervation”, in which sensations that would apparently arise within the muscles had origin in the brain, in association with motor commands. The discovery of the muscle sense is attributed to Charles Bell, in 1826. He also speculated about whether the signals were of central or peripheral origin. He questioned, “(do) muscles have any other purpose to serve than merely to contract under the impulse of their motor nerves?” He then wrote that “between the brain and the muscles there is a circle of nerve; one nerve (ventral roots) conveys the influence from the brain to the muscle, another (dorsal roots) gives the sense of the condition of the muscle to the brain.” [1] [2] [12]

Two schools of thought developed: one that supported that the muscle sense had an entirely central origin, and another that believed that the main responsible was a peripheral signal (2). Henry Bastian, the originator of the term kinaesthesis, was at the time the only who proposed a hybrid theory that encompassed both central and peripheral components. He abandoned this idea in favor of a purely peripheral mechanism [1] [2].

For much of the 20th century, the prevailing view regarding the limb position sense was that the joints where the main receptors responsible for kinaesthetic sensations. This changed after the experiments of Goodwin and colleagues on the sensory effects of muscle vibration. This study provided evidence for the role of muscle spindles in conscious sensation and currently they are considered the principal proprioceptors [2] [9] [12].

The term “proprioception” was introduced by Sherrington in 1906. The term is a combination of the Latin “propius” (one’s own) and “perception”. He described it as a type of feedback from the limbs to the central nervous system. He referred to proprioceptors as: “‘In muscular receptivity we see the body itself acting as a stimulus to its own receptors – the proprioceptors.” [1] [10] [11]

The proprioceptive senses[edit]

The proprioceptive senses include the senses of position and movement of limbs and trunk, the sense of effort, the sense of force, and the sense of heaviness. Like previously mentioned, the receptors that are involved in proprioception are located in skin, muscles, and joints [2].

When limbs move or change position, the tissues around the relevant joint are deformed. These include skin, muscles, tendons, fascia, joint capsules, and ligaments, all of which are innervated by mechanically sensitive receptors. Their density varies across muscles and different regions of the body. A specific type of receptor, the muscle spindles, play an essential role in proprioception, along with some skin receptors that provide additional information. Another receptor that contributes to proprioception is the Golgi tendon organs. These have been gaining prominence recently. They identify changes in muscle tension, and contribute to the senses of force and heaviness. In general terms, the information that is received by the receptors is sent through the spinocerebellar tract into the cerebellum. It accepts the information provided by every muscle and joint in the body, and calculates where limbs must be in space [2] [3] [11]. The sense of limb position is complex, with different sources of information interacting to produce perception, such as tactile, visual, and proprioceptive. The brain continuously matches visual and kinaesthetic inputs during movements to link what is seen with what is felt [5] [7].

Presently, regarding peripheral afferents, it is considered that “muscle spindles provide the kinaesthesia sense, Golgi tendons organs provide the sense of tension, the vestibular system provides the sense of balance, and the central nervous system provides the sense of effort. In short, limb placement is achieved by combining motor command signals and afferent signals in order to produce the best estimate of body part positioning, although how these sources of information combine to give the normal positional acuity remain the subject of further experiments [5].

Proske (2015) has proposed “the idea of the existence of two kinds of position sense, served by different classes of sensory receptors.” The first relates to signaling the position of one body part relative to another. In this case, the principal receptors are the muscle spindles, with cutaneous receptors acting as proprioceptors in a supporting role. The second kind of position sense would determine the location in space of the body or one of its parts. For this, vision would contribute the most, supported by cutaneous receptors acting as exteroceptors and auditory receptors signaling spatial information [10].

Joint and skin receptors[edit]

Joint receptors were thought to be all important in kinaesthesia, but the present view is that they only have a minor contribution. They may contribute proprioceptive information as limb displacement approaches the limits of joint movement, but not inform about position. There is evidence, however, of a contribution by joint receptors in the mid-range of movements at the finger joints [2] [7] [10].

According to Proske (2015), skin receptors can act both as proprioceptors and exteroceptors. When a joint rotates it causes the skin to stretch on one side and to be slackened or folded on the other side. These deformations will stimulate the skin mechanoreceptors, leading to sensations of elbow movement. Moreover, the elbows may come in contact with external objects, which is signaled by cutaneous receptors acting as exteroceptors. These contribute to kinaesthesia at the index finger, elbow, and knee [2] [9] [10]. In this way, the skin contributes to kinaesthesia, and the sensitivity of human skin stretch receptors is similar to that of muscle spindles afferents (when expressed as impulses per degree of joint motion) [2].

The contribution of the skin receptors to kinaesthesia is essential in the skin adjacent to the finger joints. Their presence at each finger joint allows them to provide joint-specific information [2] [7] [9]. However, the activation of cutaneous receptors can produce illusory movements of the index finger, elbow, and knee, supporting the hypothesis that cutaneous receptors can generate proprioceptive sensation at other joints beside those of the hand [9]. Therefore, skin afferents have a significant role in kinaesthesia, likely contributing to movement sensation at most joints. Nonetheless, their contribution to position sense at the more proximal joints is likely to be less relevant than the input from muscle spindles [2].

A note will be given to auditory input as an exteroceptor, with the ability to localize sounds, providing spatial information about the surroundings. Recent reports describe how hearing can affect the perceived size of a limb [10].

Some factors that can affect proprioception[edit]

Some researches indicate that pain can interfere with the perception of the position of the painful limb, although others did not find such an association between proprioception and pain. In another study, it was found that pain did not affect ankle joint position sense but that it affected the ankle movement detection threshold. This leads to the suggestion that the relationship between pain and proprioception is complex and that more research is necessary to clarify the connections between these two concepts [5].

Another factor that can impact proprioception is the increased exposure to relevant proprioceptive stimuli. This was observed in studies of visually guided reaching, where the accuracy of matching performance was improved [8].

Muscle spindles[edit]

As mentioned, muscle spindles afferents are considered to be mainly responsible for the sense of position and the perception of limb movement. They include both the primary and secondary endings of spindles. It is believed that the secondary endings signal only length changes, contributing to the sense of position since they do not have a pronounced velocity sensitivity [5] [7] [10]. Proske and Gandevia (2009) referred that “The neural basis of limb position sense is the ability of receptors like muscle spindles to maintain static levels of discharge which increase in proportion to the increase in muscle length.” [7]

Muscle spindles serves various roles in motor control, and although they are proprioceptors, they have other non-proprioceptive roles such has contributing to the reflex control of posture and locomotion [10].

Evidence[edit]

There is strong evidence in support of muscle spindles as the main proprioceptors. Their role has been studied through the illusory movement sensation paradigm, and it is based in two kinds of experiment that generate the illusion of limb displacement. First, and maybe the most important evidence, is the fact that using muscle vibration over the tendon or muscle – a selective stimulus for muscle spindles – generates illusions of limb movement and displacement, provided the muscle remains passive. This was first observed by Goodwin et al. (1972). The second piece of evidence comes from the thixotropic property of extrafusal and intrafusal muscle, meaning the dependence of passive tension in muscle on the previous history of contraction and length changes. This second method has the advantage of changing muscle spindle background activity without changing the muscle length [2] [5] [7] [10].

Further evidence has been provided by studies that use other techniques such as skin and joint anesthesia, and the disengagement of muscles from joints. For example, the sense of position and movement persisted after joint replacement. In patients that had a total hip placement, the kinaesthetic sense remained intact, pointing to the importance of muscle receptors in proprioception. It also suggest that, at least at some joints, joint receptors do not play a significant role in kinaesthesia [2] [7].

The central nervous system distinguishes between muscle spindle impulses generated by muscle stretch and by fusimotor activity, which may further indicate the prominent role of these receptors in kinaesthesia [5].

The sense of effort[edit]

Traditionally, the sense of effort, force, and heaviness have been regarded as to be generated by signals of central origin associated with motor commands. The senses of effort, force, and heaviness are distinct, has proprioceptive sensations, since they are always associated with motor commands. Kinaesthetic sensations can arise in passive limbs. Recent developments have given the centrally generated sense of effort a greater contribution to position sense. Fortier and Basset (2012) mention that the current hypothesis is that when “spindles are activated through the fusimotor system, they no longer contribute to position sense and the effort signal generated by the motor command provides the additional positional information”, and that “future experiments should concentrate on identifying the central sites of origin of the effort sensation, determining the effect of sense of effort on position sense, and assessing the interaction between peripheral and central systems.” [2] [5] [7]

The central nervous system[edit]

The central nervous system receives input from several sources like the somatosensory system, the vestibular system, and the visual system. The somatosensory system is composed by several types of receptors, like mechanoreceptors, thermoreceptors, pain receptors, and proprioceptors. The integration of proprioceptive signals by the central nervous system is still not completely understood, despite several studies on the subject matter. The traditional views are changing and some propose that the sense of position and movement results from integrating multiple sources of proprioceptive information within the central nervous system, and not just from muscle spindles [5].

Effect of exercise[edit]

The effect of exercise in the sense of position remains controversial to explain, and further research is necessary. Some studies suggest a decline of the sense of velocity and position sense after an isometric contraction exercise protocol. Indeed, there is a common feeling of awkwardness and clumsiness after intense exercise that is not only muscle weakness, but also a lesser certainty about the placement of the fatigued limbs in the absence of vision [2] [5]. There is also the suggestion that the effort that is required to maintain the position of a limb against the force of gravity is the element that provides the positional cue, although some studies contradict this sense of effort hypothesis. Moreover, data supports the view that muscle spindle would be responsible for the sense of movement, not being sensitive to exercise disruption [5].

Proprioception and virtual reality[edit]

Proprioception allows the formation of a mental model, describing the spatial and relational dispositional of the body and its parts. A virtual reality system needs that the normal proprioceptive data that is used to form a mental model of the body be overlaid with sensory data that is supplied by the computer-generated displays. For an effective virtual reality, it is fundamental that there is consistency between proprioceptive information and sensory feedback. This is done by the correct capturing of the movement of the user, and simulating it in the virtual environment, in order to increase a sense of immersion [13]. Also, according to Mine (1997), “providing a real-world frame of reference in which to operate and a more direct and precise sense of control, proprioception helps to compensate for the lack of haptic feedback in virtual-environment interaction.” [14]

References[edit]

  1. 1.0 1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8 Han, J., Waddington, G., Adams, R., Anson, J. and Liu, Y. (2016). Assessing proprioception: a critical review of methods. Journal of Sport and Health Science, 5: 80-90
  2. 2.00 2.01 2.02 2.03 2.04 2.05 2.06 2.07 2.08 2.09 2.10 2.11 2.12 2.13 2.14 2.15 2.16 2.17 2.18 2.19 Proske, U. and Gandevia, S. C. (2012). The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiological Reviews, 92: 1651-1696
  3. 3.0 3.1 Surve, S. (2009). What is proprioception? Retrieved from http://brainblogger.com/2009/06/09/what-is-proprioception
  4. 4.0 4.1 SPD Australia. The proprioceptive system. Retrived from http://www.spdaustralia.com.au/the-proprioceptive-system
  5. 5.00 5.01 5.02 5.03 5.04 5.05 5.06 5.07 5.08 5.09 5.10 5.11 5.12 5.13 Fortier, S. and Basset, F. A. (2012). The effects of exercise on limb proprioceptive signals. Journal of Electromyography and Kinesiology, http://dx.doi.org/10.1016/j.jelekin.2012.04.001
  6. Brain Balance. Proprioception explained. Retrieved from https://www.brainbalancecenters.com/blog/2015/08/proprioception-explained
  7. 7.0 7.1 7.2 7.3 7.4 7.5 7.6 7.7 7.8 7.9 Proske, U and Gandevia, S. C. (2009). The kinaesthetic senses. Journal of Physiology, 587(17): 4139-4146
  8. 8.0 8.1 Goble, D. J., Noble, B. C. and Brown, S. H. (2010). Where was my arm again? Memory-based matching of proprioceptive targets is enhanced by increased target presentation time. Neuroscience Letters, 481: 54-58
  9. 9.0 9.1 9.2 9.3 9.4 Collins, D. F., Refshauge, G. T. and Gandevia, S. C. (2005). Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. Journal of Neurophysiology, 94: 1699-1706
  10. 10.0 10.1 10.2 10.3 10.4 10.5 10.6 10.7 10.8 Proske, U. (2015). The role of muscle proprioceptors in human limb position sense: a hypothesis. Journal of Anatomy, 227: 178-183
  11. 11.0 11.1 11.2 Dover, G. and Powers, M. (2003). Reliability of joint position sense and force-reproduction measures during internal and external rotation of the shoulder. Journal of Athletic Training, 38(4): 304-310
  12. 12.0 12.1 Winter, J. A., Allen, T. J. and Proske, U. (2005). Muscle spindle signals combine with the sense of effort to indicate limb position. Journal of Physiology, 568(3): 1035-1046
  13. Slater, M., Usoh, M. and Steed, A. (1995). Taking steps: the influence of a walking technique on presence in virtual reality. ACM Transactions on Computer_Human Interaction, 2(3): 201-219
  14. Mine, M. R. (1997). Exploiting proprioception in virtual-environment interaction. PhD thesis, University of North Carolina

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