Proprioception and Clinical Correlation

Abstract

Proprioception is the sense of position or the motion of the limbs and body in the absence of vision. It is a complex system having both conscious and unconscious components involving peripheral and central pathways. The complexity of sensorimotor systems requires deep knowledge of anatomy and physiology to analyze and localize the symptoms and the signs of the patients. Joint sense and vibration sense examination is an important component of physical examination. This chapter consists anatomy, motor control, postural control related to proprioception with neurologic clinical correlation and also the information about the changes of proprioception after orthopedic surgeries and discuss with the available literature.

1. Introduction

1.1 Anatomy

Proprioception was first described by Sir Charles Bell in 1830s as sixth sense coming from Latin word proprius meaning “one’s own” and perception “perceiving one’s own self” [1]. Proprioception is generally defined as either the sense of position or the motion of the limbs and body in the absence of vision [2]. Limb position is a static sense, whereas limb motion is a dynamic sense [3]. It is described as the most important sensorial modality for the internal representation of body map providing static and dynamic proprioceptive systems [4].

Proprioception is a complex system having both conscious and unconscious components involving peripheral and central pathways. The proprioceptive sensations arise from the deeper tissues. The main receptors are muscle spindles, tendons, Ruffini endings in joint capsules ligaments and Pacinian corpuscles reacting pressure, tension, stretching or contraction. The cutaneous receptors of the skin also contribute to joint position and motion sense especially at digits, elbow and knee. The term kinesthesia is generally used to describe the conscious awareness of the body or limb position in space [1, 5, 6, 7]. Conscious proprioceptive impulses elongate along large and myelinated fibers from the peripheral nerves into the dorsal root ganglion of spinal cord (first order neurons) and then via the medial division of the posterior root, via posterior white columns of fasciculi gracilis and cuneatus and ascend to the nuclei gracilis and cuneatus in the lower medulla. Axons of the second-order neuron decussate as internal arcuate fibers (second order neurons), and then ascend in the medial lemniscus to the contralateral somatosensory region of thalamus (Figure 1) [2, 5].

The main pathway for proprioceptive information is via the dorsal column medial lemniscal, posterior and anterior spinocerebellar tracts and spinoreticular tracts [6, 7].

There is a high density of complex spindles in deeper cervical muscles particularly in the intermediate columns, acting as neck prorioceptive receptors. This system is important for head and neck position sense together with the high density muscle spindles of sub-occipital triange. The density of muscle spindles is higher in the upper cervical spine when compared with the lower cervial and cervico-thoracic and thoraco-lumbar junctions [8]. Neck proprioception plays an important role in limb coordination and body-scheme representation [8]. Proprioceptive impulses from the head and neck are supplied by cranial nerves [5].

Contralateral primary and secondary sensorimotor cortex, supplementary motor area and bilateral inferior parietal lobes and basal ganglia (especially nigrostriatal pathways, striatal neurons and putamen) are involved in processing proprioceptive information during passive movement [9, 10]. The cerebellum contributes to proprioception only during movement [3]. Especially deep medial fastigial nucleus of cerebellum converges vestibular and neck proprioceptive sensory signals describing body’s movement in space [11, 12].

1.2 Proprioception and motor control

The sensorimotor system, defined as the sensory, motor, and central integration, is a crucial and intricate component of the motor control system [13]. Motor control is a complex and dynamic process based on the selective integration of sensory information from multiple sources, motor commands, and motor output [13, 14]. There are specific unique roles associated with each sensory source (i.e., somatosensory, visual, vestibular) that cannot be compensated fully with each other [14, 15]. The environment is experienced through sensory systems: exteroception (e.g., sight, hearing, touch), interoception (e.g., arousal, pain, visceral sensations, muscular sensations), and proprioception (e.g., sense of position, motion, and force), which all required for successful motor control [16, 17]. During a task-oriented activity, motor adaptation, defined as a process of modifying the movement based on error feedback [18], skills are needed to cope with the changes occurring in the external and internal environment [2]. Motor adaptation is stimulated with sensorial triggers by using both feedback (reactive: adjust ongoing motor behavior) and feedforward (preparatory: pre-planning and anticipating the motor sequence from the previous experience) mechanism. Proprioceptive information, from proprioceptors found in muscle, tendon, ligament, capsule, skin, and fascial layers, plays an integral role in motor control and considered as multifold [14].

The role of proprioceptive information in motor control can be divided into two categories: external environment (even vs. uneven ground) and internal environment (carrying a load on shoulders vs. hands below knuckle height). The motor programs often need to be adjusted to accommodate unexpected perturbations or changes in the external environment. Although the source of this information is usually associated mainly with visual input, there are many situations where proprioceptive input is the fastest and/or most accurate. Proprioception is necessary during motion execution to update feedforward commands derived from the visual image [14]. Attention to environmental constraints is also required because dealing with complex environments often requires behavioral flexibility to maintain postural balance [19]. Secondly, the central nervous system needs an updated body schema of the biomechanical and spatial properties of body parts to plan and modify internally generated motor commands [20]. Before and during a motor command, the motor control system must consider the current and changing positions of the respective joints to account for the complex mechanical interactions within the musculoskeletal system components [14]. Additionally, proprioception is important after movement to compare the actual movement and intended movement, besides the predicted movement derived from the efference copies (corollary discharge: copying of motor commands based on past events) of motor commands, which has an essential role in motor learning to update the internal forward model of motor command [21].

1.3 Proprioception and postural control

During the execution of all motor tasks, proprioception is required to prepare, maintain, and restore the stability of both the entire body (postural equilibrium) and the segments (joint stability) [14, 15]. Postural control, defined as controlling the position of the body regarding the task in the environment, involves neural control of “postural equilibrium” and “postural orientation”. Postural equilibrium consists of the coordination of sensory and motor strategies to maintain balance by controlling the body’s center of mass (COM) over its base of support (BOS) to maintain postural stability during both intrinsic (self-initiated) and extrinsic (externally triggered) disturbances. The postural equilibrium controls stability during both static (i.e., quiet standing) and dynamic (i.e., walking and reaching) situations. Postural orientation involves positioning body alignment with respect to gravity, the support surface, visual environment, and other sensory reference frames [22].

Postural control is considered as a complex motor skill derived from the interaction of multiple sensorimotor processes, which are; biomechanical constraints (i.e., BOS, degrees of freedom, strength, limits of stability), movement strategies (i.e., reactive, anticipatory, voluntary), sensory strategies (i.e., sensory integration, sensory re-weighting), orientation in space (i.e., perception of visional verticality, perception of postural verticality), control of dynamics (i.e., gait, proactive), cognitive processing (i.e., attention, learning, reaction time), experience and practice [23]. Impairment of the proprioceptive sensation can disrupt any of these six resources, which contributes to postural control (Figure 2). “Sensory strategies” are one of the most critical issues to discuss. Sensory information from somatosensory (tactile sense and proprioception), visual and vestibular systems must be integrated to interpret complex sensory environments for achieving postural control. Depending on the environmental conditions, the relative contribution of each sensory system changes, which is referred to as “sensory re-weighting” [24]. Healthy persons rely on somatosensory (70%), vision (10%), and vestibular (20%) information when standing on a stable surface in a well-lit environment (13). On the other hand, when standing on an unstable surface, due to decreased dependence on surface somatosensory inputs for postural orientation, they need to increase sensory weighting to vestibular and visual information [25]. The dynamic regulation or re-weighting of sensory cues is essential for maintaining postural stability when moving between different environments requiring distinct sensorial systems, such as different surfaces (i.e., walking on the sidewalk, walking on grass) or different lighting (i.e., moving in a well-lit room, moving in a dark room) [23]. The interplay between these three sensory modalities is critical for accurate estimates of self-motion and postural control [26].

Figure 1.

Neuroanatomic pathway adopted from DeJong’s the neurologic examination.

Besides different sensory cues, different mechanical conditions provide significant advantages to humans for maintaining upright standing [27]. Decreased proprioception could lead to “biomechanical constraints” such as abnormal joint biomechanics and decreased muscle strength [28, 29], leading to postural dyscontrol. The “control of dynamics” is defined as the ability to perceive body segments relative to one another to stabilize the COM. Maintaining COM requires input from multiple sensory systems, sensorial re-weighting, and multisensory integration to calculate body state, including the COM and heading [30]. “Movement strategies” (i.e., postural sway, ankle strategy, hip strategy) can be used to return the body to equilibrium in a stance position [23]. Without proprioceptive input from the ankle and knee, ankle muscle responses are delayed suggesting that lower leg balance correcting responses are triggered by hip and, possibly, trunk proprioceptive inputs. Especially hip muscle proprioceptive inputs, considered critical for automatic balance correcting responses [31]. Additionally, cervical proprioception is of particular importance for “orientation in space”. Neck muscle inflow has effects on the perception of body orientation and motion. Prolonged, intense proprioceptive input from neck muscles can induce persistent influences on self-motion perception and cognitive body representation [32]. The loss of proprioception could also impact the “cognitive processing” specifically the reaction time, and other factors such as attention, memory, and visuospatial abilities may contribute to spatial cognitive skills (Figure 2) [23].

Figure 2.

Adapted from the framework of the six important resources required for postural control system by Horak, 2006 [23], the contribution of proprioception sensation to postural control.

2. Clinical implications and evaluation of proprioception

The loss of proprioceptive afferents may affect the control of muscle tone, disrupts postural reflexes, and severely impairs spatial and temporal aspects of movement [33]. Proprioceptive impairments are associated with various neurological conditions such as stroke [34], Parkinson’s disease [35], peripheral neuropathy [36], as well as orthopedic conditions such as low back pain [37], neck pain [38], sports injuries like chronic ankle instability [39], ACL injuries [40], post-operatively such as mastectomy [41], knee arthroplasty [42], and aging [43]. Considering the importance of proprioception for motor control, a detailed evaluation of proprioceptive sense and application of treatment approaches focusing on training the proprioceptive sense is important for restoring motor function. Proprioception can be measured by using specific and non-specific tests in clinical practice.

Specific Tests of Proprioception: assess an individual’s status regarding the joint position sense and kinesthesia [21]. Joint position sense tests assess precision or accuracy in repositioning the joint at a predetermined target angle and can be measured as active joint position detection (AJPD) [e.g., position matching task, position copying task] and passive joint position detection (PJPD) [e.g., thumb finding test, dual-joint position test] [44]. Kinesthesia tests assess the ability to perceive joint movement. For evaluating the perceptual aspect of proprioception, psychophysical thresholds represent the gold standard [33]. These tests are usually performed passively and can be measured by using passive motion detection threshold (PMDT) and passive motion direction discrimination (PMDD) [e.g., distal proprioception test, Rivermead Assessment of Somatosensory Perception] [44].

Non-specific Tests of Proprioception: for determining the contribution of proprioceptive signals on balance control, functional balance tests can be used to provide an estimate of potential proprioceptive disturbances [33]. These tests involve all body and other sensory and motor functions; therefore, they are considered non-specific tests of proprioception [21]. Balance tests can be modified to challenge proprioception, such as unilateral/bilateral stance with eyes open/closed, different supporting surfaces (i.e., stable or unstable), and with/without perturbations [44, 45]. Stereognosis and skilled motor function tests are important as they indicate the contribution of proprioceptive system in the performance of many activities of daily living [46].

3. Neurologic correlation

The complexity of sensorimotor systems requires deep knowledge of anatomy and physiology to analyze and localize the symptoms and the signs of the patients. Joint sense and vibration sense examination is an important component of neurological examination.

The classic diseases causing sensory ataxia are tabes dorsalis, polyneuropathies (especially involving large fibers), dorsal root ganglionopathies and subacute combined degeneration. With parietal lobe lesion, position sense is often impaired and vibration preserved [5]. Vibratory sensation may also be impaired in lesions of the peripheral nerves, plexopathies, radiculopathies, dorsal root ganglion, posterior columns and medial lemniscus. In patients with peripheral neuropathies, vibration sensation is lost in the lower extremities first. Impaired vibration from posterior column disease is more likely to be uniform at all sites in the involved extremities. In spinal cord diseases, detecting a “level” of vibration sensory (segmental demarcation) loss over the spinous processes is crucial for diagnosis [5]. In patients with diabetic neuropathy, the decline in proprioceptive function may be caused by impairment in muscle spindle function and or the spindle receptors itself [47].

In patients with hereditary sensory and autonomic neuropathy type III patients (Riley-Day Syndrome, familial dysautonomia) ataxic gait is explained by poor proprioceptive acuity at the knee joint [48]. In mitochondrial ataxias sensory ataxia (which classically include gait ataxia worsened by loss of visual fixation) is due to the involvement of proprioception, secondary to peripheral neuropathy or neuronopathy [49]. In patients following whiplash type injuries involving soft tissues of cervical spine leads to proprioceptive deficits affecting head and position sense. Also in patients with chronic whiplash associated disorders are reported to have balance and dizziness problems, head and eye movement impairments reflecting mismatch od afferent input from the proprioceptive, visual and vestibular systems [8, 50]. Lesions of the dorsal columns impairs sensation of touch, vibration and proprioception in the ipsilateral side of the body below the injury level [51]. In patients with non-specific low back pain, postural control is impaired during standing and slow performance movements. This is due to an altered use of ankle compared to back proprioception related activity in right primary motor cortex and frontoparietal cortex [52]. Brainstem lesions resemble those in spinal cord disease as it selectively involves spinothalamic tract or medial lemniscus causing contralateral loss of position sense and vibration sense [5].

Neglect is a condition in which patients loose self-spatial awareness opposite to the damaged site of the brain. It is proposed that it is associated with the lesions of the dorsal stream causing dysfunction of proprioceptive space which is encoded in the bilateral parietal cortex [53]. Loss in the position sense may cause pseudochoreoathetosis as well. This abnormal involuntary, spontaneous movements are restricted to the parts with proprioceptive sensory loss. It is proposed that failure to integrate cortical proprioceptive sensory inputs in striatum may explain this situation [5, 54].

There are experimental evidence of proprioception impairments in Parkinson’s disease. Parkinsonian gait is affected by the involvement of lower limb proprioceptive deficits as well as the involvement contralateral somatosensory and premotor lateral cortices and posterior cingulate cortex and basal ganglia and bilateral prefrontal cortex [10, 55, 56]. It was also shown that conscious perception of kinaesthetic stimuli is impaired in Parkinson’s disease as cerebro-basal loops are not intact [9].

Weeks and colleagues showed that patients with cerebellar damage had reduced dynamic proprioceptive acuity which was also parallel to their motor deficits [3]. Diseases of the primary somatosensory cortex do not generally produce sensory symptoms but deteriorate fine and delicate manipulations in the contralateral part depending on position sense [2, 5]. Many patients with stroke experience proprioceptive deficits. Recovery of proprioception increases in the chronic phase [57, 58]. In study by Pope it was shown that proprioceptive input from the neck also may change cerebellar output affecting M1 plasticity [59]. In the study of Vidoni and colleagues preserved motor learning after stroke was related to the degree of proprioceptive deficit suggesting the relation between proprioceptive perception from muscle spindles and motor learning and central neuroplasticity [58, 60].

4. Proprioception after orthopedic surgeries

Studies on changes in joint proprioception after orthopedic surgeries are available in the literature. This section consists of the information in the literature about our five major joints.

4.1 Knee joint

Knee proprioception is necessary to achieve normal joint coordination during movement as well as providing joint stabilization [61, 62]. The anterior cruciate ligament (ACL), posterior cruciate ligament, collateral ligaments and menisci contribute to proprioception with the help of proprioceptors they have [63, 64]. The mechanoreceptors of the cruciate ligaments, together with the mechanoreceptors of the joint capsule, transmit information about the extension and flexion of the knee joint to the brain [65].

The ACL is the most important ligament involved in knee mechanical and neuromuscular stability. It contributes to proprioception in joint movement. However, the ACL is the most frequently injured ligament. After ACL rupture, knee proprioception is disrupted [66, 67].

Various autografts and allografts are used for ACL reconstruction. Patellar tendon or hamstring tendons may be preferred in patients using autografts. In addition, different techniques and materials are used. However, there is no gold standard in graft and technique selection [68]. In order for ACL reconstruction to be successful, not only mechanical but also neuromuscular stability is required. Neuromuscular stability depends on obtaining proprioception [69]. ACL injury leads to degradation of mechanoreceptors and a histologic study revealed that free nerve endings disappear after 1 year [70]. The effectiveness of ACL reconstruction in regaining proprioception has been tried to be revealed by some studies [71, 72, 73, 74]. While some studies argue that ACL reconstruction is not sufficient to restore joint position [71, 72, 73], some studies advocate the adverse opinion [74]. The lack of a test to distinguish about whether the proprioception is derived from the soft tissues around the knee and capsule or from mechanoreceptors on ACL prevents to reach a certain decision about the mechanoreceptors of ACL [75].

Even after total knee arthroplasty, the contribution of the soft tissues around the knee to proprioception continues. In order to take advantage of this effect and ensure satisfactory outcomes in these patients, the soft tissue and gap must be well adjusted. Unicompartmental replacement protecting the ACL may be more advantageous in not reducing proprioception due to the proprioceptive effect of ACL. Also Ishii et al. [76] conclude that balance is improved after the postoperative period in bilateral total knee arthroplasty. It is stated that the first 6-week period is the critical period for adaptation time and proprioceptive loss after total knee replacement, and a new pattern in the knee load distribution occurs with postoperative rehabilitation [77].

4.2 Hip joint

Loss of proprioception, balance, sensation as joint position and kinesthetic are frequently observed in patients with knee osteoarthritis [78, 79]. Shakoor et al. [80] described significant sensory deficits associated with hip osteoarthritis, and these deficiencies involved both upper and lower limbs. The mechanism for this remains unclear; however, it has been suggested that there may be neurological feedback mechanisms or a inherent generalized neurological defect [78].

The greatest portion of mechanoreceptors and free nerve endings and highest concentration of pain receptors are located in the anterosuperior, posterosuperior and anterolateral labrum, respectively [81, 82].

There is no satisfactory information about proprioception impairment after surgeries due to hip pathologies. In the literature on the relationship between arthroplasty and proprioception, there are studies related to the knee rather than the hip. Interestingly, Ishii et al. [83] found no difference in proprioceptive responses among participants in the total hip arthroplasty, hemiarthroplasty and healthy control groups. They thought that the mechanoreceptors in the muscles, tendons and ligaments were responsible for joint proprioception rather than the intracapsular structures. While capsular receptors play a secondary role, muscle receptors play a primary role in hip proprioception. Therefore, it has been suggested that proprioception does not decrease after surgery, despite the capsule being removed during arthroplasty [84].

The effects of FAI and labral tear treatments on proprioception are not well known, but due to their proprioceptive properties, hip musculotendinous and capsuloligamentous tissues contribute to lower limb posture and stabilization through neuromuscular control. Therefore, preserving proprioceptive tissues as much as possible will prevent lower extremity injuries in arthroscopy operations.

4.3 Ankle joint

Ankle injuries are in the first place in sports-related injuries and lateral ankle sprains constitute the majority of this [85]. Unfortunately, many of these acute injuries can become chronic [86, 87]. Training, fatigue, and ankle injuries can affect ankle proprioception. Joint position sense, peroneal reaction time, EMG evaluation of peroneal muscles, and balance tests are tools to evaluate proprioception before and after ankle injuries or surgeries.

There are two important anatomical structures that provide proprioception and are located around the foot and ankle. Superior and inferior extensor retinaculum act as a pulley protecting tendons close to bony structures. The lateral ankle complex is the other anatomical structure with proprioceptive properties [88, 89]. Both acute and chronic injuries of the ankle can predispose the proprioceptors of the ankle. The differentiation in proprioception after these injuries were presented in the literature. While Vries et al. [90] stated that there was no difference between chronic ankle injury, acute trauma and healthy control groups, there are studies suggested that proprioception after acute inversion injuries and chronic ankle injuries are decreased [91, 92, 93]. Recovery of the proprioception is crucial after ankle injuries to maintain balance control. In order to achieve this, rehabilitation should not be neglected, especially after lateral ankle sprains.

A study conducted by Conti et al. [94] found no difference in proprioception between operated and non-operated side in total ankle arthroplasty. However, ankle arthroplasty has the worst outcome in terms of proprioception and balance compared to total hip and knee arthroplasty [95].

4.4 Shoulder joint

Some studies have revealed Pacinian corpuscles and Golgi tendon organ with mechanoreceptors in the shoulder [96, 97]. However, they discovered that while there are free nerve endings in the labrum and subacromial bursa, these structures do not contain mechanoreceptors. It is also thought that the supraspinatus muscle has more receptors than the infraspinatus muscle contains [98].

The pathological conditions of the shoulder joint can affect shoulder proprioception. Surgical shoulder diseases include rotator cuff tears, subcacromial pathologies, biceps tendon diseases and instabilities. Studies comparing pre- and post-surgical proprioception in the shoulder joint are not sufficient. In a study conducted by Aydın et al. [99], it was revealed that there was no difference in terms of proprioception between surgically treated and non-surgically treated shoulders in cases of instability. Duzgun et al. [100] stated a rapid recovery in shoulder joint proprioception after rotator cuff surgery as their experience.

Shoulder arthroplasty is thought to negatively affect proprioception. It has been stated that intervention to the subscapularis muscle and glenohumeral ligaments during shoulder arthroplasty may be effective in this decrease in proprioception [101, 102].

4.5 Elbow joint

Soft tissue damage is significant in elbow arthroplasty. Both flexor and extensor muscles are affected, collateral ligaments are released and capsule is removed. Therefore, the proprioceptive tissues as like skin, capsule, muscle and tendons are damaged. Despite the role of proprioception is still not well-established, one study was found an impairment in proprioception after total elbow arthroplasty [103].

In conclusion, proprioception may be adversely affected after joint surgeries. It should definitely be included in the rehabilitation program considering this situation. Proprioception seems to be an important factor for gaining balance and gait speed, especially after arthroplasties in the lower extremity.

Conflict of interest

The authors declare no conflict of interest.