CHAPTER 33

The Proprioceptive Sensations

The proprioceptive sensations arise from the deeper tissues of the body, principally from the muscles, ligaments, bones, tendons, and joints. Proprioception, or kinesthesia, refers to either the sense of position of a body part or motion of a body part. Proprioception has both a conscious and an unconscious component. The conscious component travels with the fibers subserving fine, discriminative touch; the unconscious component forms the spinocerebellar pathways. The conscious proprioceptive sensations that can be tested clinically are motion, position, vibration, and pressure.

Anatomy

The primary receptors for proprioception are the muscle spindles. Other peripheral sense organs dealing with proprioception are located in the muscles, tendons, and joints, particularly pacinian corpuscles. These respond to pressure, tension, stretching or contraction of muscles fibers, joint movement, changes in the position of the body or its parts, and related stimuli. Cutaneous afferents play a contributory role. Proprioceptors are essential for the normal coordination and grading of muscle contraction and the maintenance of equilibrium. Conscious proprioceptive impulses travel along large, myelinated fibers from the periphery to the first-order neuron in the dorsal root ganglion (DRG) and then via the medial division of the posterior root (Figure 32.1). These fibers then enter, without a synapse, the ipsilateral fasciculi gracilis and cuneatus and ascend to the nuclei gracilis and cuneatus in the lower medulla, where a synapse occurs. The spinocervical and dorsal spinocerebellar tracts also convey proprioceptive impulses.

Axons of the second-order neuron decussate as internal arcuate fibers and then ascend in the medial lemniscus (ML) to the thalamus (Figure 33.1). The somatotopic organization in the posterior columns and lemniscal pathways is the same as for light touch (Figure 32.3). Other DRG fibers subserving kinesthesia synapse in the dorsal horn and then ascend in the dorsolateral funiculus to the lateral cervical nucleus, where they join the ML. The thalamoparietal radiations then go through the posterior limb of the internal capsule, and the fibers are distributed to the cortex.

FIGURE 33.1 The pathways for position sense and fine discriminative touch through the posterior columns and medial lemniscus.

Proprioceptive impulses from the head and neck enter the central nervous system with the cranial nerves. Many terminate on the mesencephalic root of the trigeminal nerve; others accompany motor nerves from the muscles they supply. Impulses probably reach the thalamus through the ML. Recently, the higher cognitive neurophysiology for position sense was described by researchers who were awarded the Nobel prize in Medicine for their work. Grid cells in the medial entorhinal cortex create a neural representation of space, which was popularly referred to as the brain’s internal GPS.

Senses of Motion and Position

The sense of motion, also known as the kinetic or kinesthetic sense, or the sensation of active or passive movement, consists of an awareness of motion of various parts of the body. The sense of position, or posture, is awareness of the position of the body or its parts in space. These sensations depend on impulses arising as a result of motion of the joint and of lengthening and shortening of the muscles. Motion and position sense are usually tested together by passively moving a part and noting the patient’s appreciation of the movement and recognition of the direction, force, and range of movement; the minimum angle of movement the patient can detect; and the ability to judge the position of the part in space.

In the lower extremity, testing usually begins at the metatarsophalangeal joint of the great toe, in the upper extremity at one of the distal interphalangeal joints. If these distal joints are normal, there is no need to test more proximally. Testing is done with the patient’s eyes closed. It is extremely helpful to instruct the patient, eyes open, about the responses expected before beginning the testing. No matter the effort, nonsensical replies are frequent. The examiner should hold the patient’s completely relaxed digit on the sides, away from the neighboring digits, parallel to the plane of movement, exerting as little pressure as possible to eliminate clues from variations in pressure. If the digit is held dorsoventrally, the grip must be firm and unwavering so that the pressure differential to produce movement provides no directional clue. The patient must relax and not attempt any active movement of the digit that may help to judge its position. The part is then passively moved up or down, and the patient is instructed to indicate the direction of movement from the last position (Figure 33.2). Even when instructed that the response is two alternative, forced choice, up or down, some patients cannot be dissuaded from reporting the absolute position (e.g., down), even if the movement was up from a down position; a surprising number insist on telling the examiner the digit is “straight” when it is moved into that position. It is often useful simply to ask the patient to report when he first detects movement and then move the digit up and down in tiny increments, gradually increasing the excursion until the patient is aware of the motion. Quick movements are more easily detected than very slow ones; attempt to make the excursions over about 1 to 2 seconds. Healthy young individuals can detect great toe movements of about 1 mm, or 2 to 3 degrees; in the fingers, virtually invisible movements degree or less, at the distal interphalangeal joint are accurately detected. There is some rise in the threshold for movement and position sense with advancing age. To quantitate proprioception at the bedside, move the joint (toe, finger, ankle, etc.) four times and record the proportion of correct responses.

FIGURE 33.2 Method of testing position sense, done similarly with toe.

Minimal impairment of position sense causes first loss of the sense of position of the digits, then of motion. In the foot, these sensations are lost in the small toes before they disappear in the great toe; in the hand, involvement of the small finger may precede involvement of the ring, middle, or index finger or thumb. Loss of small movements in the midrange is of dubious significance, especially in an older person. Loss of ability to detect the extremes of motion of the great toe is abnormal at any age. Errors between these two extremes require clinical correlation. If the senses of motion and position are lost in the digits, one should examine more proximal joints, such as ankle, wrist, knee, or elbow. Abnormality at such large joints is invariably accompanied by significant sensory ataxia and other neurologic abnormalities.

Position sense may also be tested by placing the fingers of one of the patient’s hands in a certain position (e.g., the “OK” sign) while his eyes are closed and then asking him to describe the position or to imitate it with the other hand. This is sometimes referred to as parietal copy because both parietal lobes (and their connections) must be intact: one side to register the position and the other side to copy it. The foot may be passively moved while the eyes are closed, and the patient asked to point to the great toe or heel. With the hands outstretched and eyes closed, loss of position sense may cause one hand to waver or droop. One of the outstretched hands may be passively raised or lowered, and the patient asked to place the other extremity at the same level. One hand may be passively moved, with eyes closed, and the patient asked to grasp the thumb or forefinger of that hand with the opposite hand. Abnormal performance on these latter tests does not indicate the side of involvement when a unilateral lesion is present.

Loss of position sense may cause involuntary, spontaneous movements (pseudoathetosis, Figure 30.8). Pseudoathetosis can occur because of severe proprioceptive loss in juvenile vitamin E deficiency. Reduction in the ability to perceive the direction of passive skin movement may indicate impairment of position sense superficial to the joint. Such impairment is usually associated with joint-sense deficit as well. The methods available for evaluating the senses of motion and position are all relatively crude, and there may be functional impairment not adequately brought out by the testing procedures.

Normal coordination requires intact proprioceptive sensory function in order to keep the nervous system informed about the moment-to-moment position of the limbs and body in space. Patients with severe proprioceptive deficits (akinesthesia) may have ataxia and incoordination, which closely resembles that seen in cerebellar disease, except that it is much worse when the eyes are closed. The incoordination due to proprioceptive loss is referred to as sensory ataxia. The ataxia and incoordination are significantly influenced by vision. Visual input allows for conscious correction of errors and permits the patient to compensate to some degree for the proprioceptive loss. There may be some degree of incoordination with eyes open, but performance is significantly degraded with eyes closed. The incoordination may be apparent on the tests usually employed for cerebellar function, such as finger to nose and heel to shin. When trying to stand and walk, the patient with sensory ataxia may not be aware of the position of his feet or the posture of his body. He may walk fairly well with eyes open, but with eyes closed, he staggers and may fall. Although the standing posture with eyes open is stable, with eyes closed, there is a tendency to sway and fall. The Romberg test explores for imbalance due to proprioceptive sensory loss. The patient is able to stand with feet together and eyes open but sways or falls with eyes closed; it is one of the earliest signs of posterior column disease. The gait of sensory ataxia and the Romberg sign are discussed in more detail in Chapter 44. A classic disease causing sensory ataxia, now seldom seen, is tabes dorsalis. Sensory ataxia is currently more likely to be encountered in patients with severe peripheral neuropathy (especially if it involves large fibers), dorsal root ganglionopathy, or vitamin B₁₂ deficiency. Profound proprioceptive loss that extends from toes to knees and fingers to elbows should raise the suspicion of dorsal root ganglionopathy (sensory neuronopathy) due to a remote effect of cancer.

Sense of Vibration (Pallesthesia)

Vibratory sensation is the ability to perceive the presence of vibration when an oscillating tuning fork is placed over certain bony prominences. For clinical purposes, it can be considered a specific type of sensation, but more probably results from a combination of other sensations. Bone may act largely as a resonator. The receptors for vibratory stimuli are primarily the very rapidly adapting mechanoreceptors such as Pacinian corpuscles, located deep in the skin, subcutaneous tissues, muscles, periosteum, and other deeper structures of the body; and Merkel disk receptors and Meissner corpuscles in the more superficial skin layers. The Merkel disk receptors and Meissner corpuscles respond best to relatively low frequencies and Pacinian corpuscles to higher frequencies. The oscillations of the tuning fork invoke impulses that are coded so that one cycle of the sinusoidal wave produces one action potential. The frequency of action potentials in the afferent nerve fiber signals the vibration frequency. The intensity of vibration is related to the total number of sensory nerve fibers activated.

Impulses are relayed with the proprioceptive and tactile sensations through large, myelinated nerve fibers and enter the spinal cord through the medial division of the posterior root. Vibration had been traditionally considered to ascend the spinal cord with other proprioceptive impulses in the dorsal columns, but likely other pathways are involved, particularly the posterior portion of the lateral funiculus. On entering the spinal cord, some fibers turn upward in the posterior columns. Others bifurcate, sending one branch into the deeper layers of the posterior horn and another into the posterior columns. Axons of the second-order neurons in the posterior horn ascend in the spinocervical tract in the ipsilateral dorsolateral funiculus and terminate in the lateral cervical nucleus. Axons from neurons in the lateral cervical nucleus cross in the anterior commissure and ascend to the medulla where they join the ML. The fibers in the dorsolateral funiculus may be the most important pathway subserving vibratory sensation in man. This divergence of the position sense and vibration sense pathways may partially explain the dissociation occasionally encountered clinically between changes in position sense and vibration sense. In subacute combined degeneration, it is not uncommon for vibration loss to be much worse than position sense loss, conversely for tabes dorsalis. With a parietal lobe lesion, position sense is often impaired and vibration preserved. Thalamocortical fibers from the ventral posterior lateral and the ventral posterior medial nuclei project to the primary somatosensory areas in the postcentral gyrus and terminate on vibration-responsive neurons.

A tuning fork of 128 Hz, with weighted ends, is most frequently used. Sensation may be tested on the great toes, the metatarsal heads, the malleoli, the tibia, anterior superior iliac spine, sacrum, spinous processes of the vertebrae, sternum, clavicle, styloid processes of the radius and ulna, and the finger joints. It is possible to test vibration perceived from the skin by testing on the pads of the fingertips or even on the skin overlying muscle and other tissues. Both the intensity and duration of the vibration perceived depend to a great extent on the force with which the fork is struck and the interval between the time it is set in motion and the time of application. Devices for measuring vibratory sensation quantitatively are commercially available; the primary applicability is in the evaluation and management of patients with peripheral neuropathy. Because of time and expense, quantitative vibratory testing (QVT) is reserved for special situations and routine clinical testing is most often employed.

For clinical testing, the tuning fork is struck and placed on a bony prominence, usually the dorsum of the interphalangeal joint of the great toe initially and held there until the patient no longer feels the vibration. Testing should compare side to side and distal to proximal sensation. If vibration is absent distally, the stimulus is moved proximally to the metatarsophalangeal joints, then the ankle, then the knee, then the iliac spines, and so forth. Upper extremity areas frequently tested include the distal joints of the fingers, the radial and ulnar styloids, the olecranon, and the clavicles. Gradual loss of sensation, such as from toe to ankle to knee, favors a peripheral nerve problem. Uniform loss of vibration beyond a certain point, for example, the iliac crests, favors myelopathy. In some patients with myelopathy, a “vibration level” can be detected by placing the fork on successively more rostral spinous processes.

A frequent problem is failure to adequately instruct the patient in the desired response. The novice examiner strikes the tuning fork, touches it to the patient’s great toe, and says, “Do you feel that?” A deceptive problem lies in the definition of “that.” A patient with absent vibratory sensation may feel the touch of the handle of the tuning fork, misinterpret it as the “that” inquired about, and respond affirmatively. Thus, very gross defects in vibratory sensibility may be completely missed. Always set the fork in motion, touch it to some presumably normal body part, and tell the patient “this is vibrating or buzzing”; then dampen the tines, reapply the stimulus, and tell the patient “this is just touching,” or something similar that clearly differentiates the nature of the two stimuli; and then proceed with the testing with the patient’s eyes closed.

With normal vibratory sensation, the patient can feel the fork over the great toe until it has almost stopped vibrating. If vibration is impaired, when the fork is no longer perceptible distally, it is moved to progressively more proximal locations until a level is found that is normal. It is also important to compare pallesthesia at homologous sites on the two sides. Sensing the vibration briefly when moving to one side after vibration has ceased on the other side is not abnormal; it probably has to do with sensory adaptation. Consistent asymmetry of vibratory sensation is abnormal; feeling the vibration for more than 3 to 5 seconds on one side compared to the other is probably abnormal. The most subtle abnormality would be to fail to feel the vibration briefly when moving from the normal to the abnormal side but not vice versa. It is important to include occasional control applications, striking the fork so the patient hears the hum, and then quickly grabbing and damping the tines before applying the handle. The patient who then claims to feel the vibration has not understood the instructions. Occasional peripheral neuropathy patients with constant tingling in the feet may think they feel a vibration even when the fork is silent.

The threshold for vibratory perception is normally somewhat higher in the lower than in the upper extremities. There is progressive loss of vibratory sensibility with advancing age, and the sensation may be entirely absent at the great toes in the elderly. The best control is an approximately age-matched normal, such as the patient’s spouse. If patient and examiner are about the same age, the examiner can compare the patient’s perception of vibration with his own.

Vibration is a sensitive modality because the nervous system must accurately perceive, transmit, and interpret a rapidly changing stimulus. An early physiologic change due to demyelination is prolongation of the nerve refractory period, which causes an inability of the involved fiber to follow a train of impulses. The ability to follow a train of stimuli is one of the first functions impaired when there is demyelination in the nervous system, either peripheral or central. Testing vibratory sensibility measures this functional ability, and loss of vibratory sensation is a sensitive indicator of dysfunction of the peripheral nervous system or the posterior columns, especially when there is any degree of demyelination.

Vibratory sensation can be quantitated fairly simply by noting where the patient can perceive it and for how long (e.g., “absent at the great toes and first metatarsal heads, present for 5 seconds over the medial malleoli [128 Hz fork]”). If the patient returns having lost vibration over the malleoli, then the condition is progressing. If on follow-up, vibration is present for 12 seconds over the malleoli and can now be perceived for 3 seconds over the metatarsal heads, then the patient is improving.

In a large series of patients, routine clinical testing was compared to QVT. Neuromuscular physicians more often overestimated than underestimated vibratory loss when compared to QVT. The graduated Rydel-Seiffer tuning fork provides a more quantitative assessment of vibratory sensation (Figure 33.3). This method is no more time consuming than routine qualitative vibratory testing, and some have suggested it replace traditional testing (see Video Link 33.1). The results correlate with more expensive and time-consuming QVT. In a series of 184 subjects, quantitative vibration testing with the Rydel-Seiffer fork correlated with the amplitude of the sural sensory nerve action potential recorded electrophysiologically.

FIGURE 33.3 A. Rydel-Seiffer tuning fork. B. Fork in motion; arbitrary scale from 0 to 8 at rest (right). The intersection of the two virtual white triangles moves up from 0 to 8 with decreasing vibration amplitude of the arms (left to right). (Reprinted from Pestronk A, Florence J, Levine T, et al. Sensory exam with a quantitative tuning fork: rapid, sensitive and predictive of SNAP amplitude. Neurology 2004;62[3]:461–464, with permission.)

Vibratory sensation may be impaired or lost in lesions of the peripheral nerves, nerve roots, DRG, posterior columns, and lesions involving the ML and other central connections. In patients with posterior column or peripheral nerve disease, vibratory sensation is lost in the lower extremities much earlier than in the upper. The finding of a normal vibratory threshold in the distal lower extremities usually obviates the need for testing proximally or in the upper extremities, absent specific symptoms involving these areas. A moderate decrease in vibratory perception in the lower extremities or a difference between the lower and the upper extremities may be clinically significant. Marked vibratory loss distally (e.g., the toe), with a transition to normal more proximally (e.g., the knee), is more consistent with peripheral neuropathy. Impaired vibration from posterior column disease is more likely to be uniform at all sites in the involved extremities. Occasionally, in localized spinal cord lesions, a “level” of vibration sensory loss may be found on testing over the spinous processes. Loss of position sense and vibration sense does not always parallel one another, and in some clinical conditions, one is affected much more and much earlier than the other. Because bone is such an efficient resonator, occasional patients with severe deficits to vibration in the distal lower extremities may feel transmitted vibrations in the hip and pelvis. When vibration seems more intact than it should, ask the patient where he feels the sensation.

Pressure Sensation

Pressure or touch-pressure sensation is closely related to tactile sense but involves the perception of pressure from the subcutaneous structures rather than light touch from the skin. It is also closely related to position sense and is mediated via the posterior columns. Pressure sense is tested by a firm touch on the skin or by pressure on deep structures (muscle masses, tendons, nerves), using finger pressure or a blunt object. The patient should both detect and localize the pressure. Strong pressure over muscles, tendons, and nerves tests deep pain sensibility.

Deep Pain Sense or Pressure Pain

Pain originating from the deeper tissues of the body is more diffuse and less well localized than superficial pain. The pathways for deep pain are the same as for superficial pain. Deep pain may be tested by squeezing muscles, tendons, or the testicles; by pressing on superficial nerves or on the eyeballs; or by pushing a finger interphalangeal joint into extreme, forced hyperflexion. Firm pressure on the base of a nail with a hammer or tuning fork handle also hurts a great deal. Loss of deep pain sensibility is a classic finding in tabes dorsalis, because of involvement of the DRG. The response to superficial or deep pain stimulation may be simply delayed before it is lost. Abadie’s sign is the absence of pain on squeezing the Achilles tendon, which is normally quite uncomfortable, Biernacki’s sign is the absence of pain on pressure on the ulnar nerve, and Pitres’ sign is loss of pain squeezing the testicles; all these are classic signs of tabes dorsalis.

Video Links

Video Link 33.1. The Rydel-Seiffer quantitative tuning fork. http://neurosigns.org/wiki/Vibration_testing_with_the_Rydel-Seiffer_tuning_fork

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