Summary

Kinesthesia. III. Kinesthetic perceptions

At the perceptual level the collections of kinesthetic sensory data from throughout the body are integrated into distinct kinesthetic perceptual systems of:

1. balance and equilibrium,
   
2. self-motion,
   
3. limb–motion,
   
4. limb position, and
   
5. force or exertion.
   

Kinesthetic perceptions are rarely derived from a single sensory organ located in one part of the body. Instead, sensory data from many types of receptors is integrated into a single kinesthetic perception. The variety of receptors contributing to kinesthesia provides sensory redundancy so that if one group of receptors fails to function another group can still provide the necessary information.

This section reviews how particular stimulation are derived into particular types of perceptions. Types of kinesthetic perceptions distinguished here include the sense of balance or equilibrium; the sense of linear, rotary, or circular self-motion; limb position sense; limb movement sense; and the sense of force or exertion.

Sense of Balance, Equilibrium.

The sense of balance is closely related to the perception of the gravitational vertical which is most readily sensed by the vestibular otolith organs. Also, the physical weight of the body and its gravitational alignment through the joints (translated from the upper-most to the lower-most body-parts) is sensed by pressure-sensitive joint receptors throughout the body (Clark, 1975) and the entire weight of the body is sensed by pressure-sensitive skin receptors against the ground.

The alignment of the body-weight relative to gravity may also be sensed by tension-sensitive tendon receptors. That is, the closer the body alignment to the gravitational vertical, the more equal the tension between opposing tendons. Though, prolonged periods of adaptation to an off-vertical position may create a somatic misperception of vertical since the receptors have become so “used to” the off-vertical alignment. When this subject’s body is placed into gravitational alignment the subject will (mistakenly) perceive that they are out of line with gravity because their somatic receptors have become so adapted to the off-vertical alignment.

Visual field motion (or non-motion) may be the most important for the sense of balance as anyone can testify who tries to stand on one leg with their eyes closed. Posture is most stable when the eyes are focused on a fixed point (Hellebrandt and Franseen, 1943). Visual field motion which occurs when a subject sways or falls off of balance will induce reflex motor reactions to counter the sway and maintain balance. When this type of visual field motion is artificially induced with a “swinging room”* infants will fall over (Lee and Aronson, 1974) and adults will experience body sway (Lishman and Lee, 1973), especially in unusual stances (Lee and Lishman, 1975). Similar postural sway will occur when projections of moving visual scenes are presented to subjects’ peripheral visual field (Lestienne et al., 1977).
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* The “swinging room” moves around the subject while the floor remains stable. Thus the subject experiences visual field motion but no accompanying stimulation from somatic or vestibular receptors (pictured by Lishman and Lee, 1973, p. 289).
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Maintenance of equilibrium through visual field stimulation is most effective with a textured visual stimulus whereby even slight lateral visual field motion can be readily detected (viz. a texture of vertical lines is more effective than horizontal lines), and this texture is most effective when presented to the peripheral visual field (Amblard and Carblanc, 1980).

Sense of Self-Motion.

The term “self-motion” is used here to refer to motion which either 1) translates the entire body in a straight line through space to a new location (linear self-motion), 2) turns the entire body around an axis (rotary self-motion), or 3) a combination of translation and rotation (circular self-motion). In contrast, “limb–motion” refers to the motion of body-parts relative to other body-parts (see Longstaff, 1996, sec. IIA.32).

Limb-motion often occurs together with self-motion (eg. motion of the limbs while walking) but the two can also be separated (eg. self-motion forward while riding in a train with the limbs held still). When self-motion occurs by riding on a train, boat, elevator, etc. without any active participation by limb-motion it is referred to as “passive movement” (Rock, 1968) or “passive locomotion” (Johansson, 1977). Three types of self-motion will be considered here; linear self-motion, rotary self-motion, and circular self-motion (For reviews see: G. J. Andersen, 1986).

- Sense of linear self-motion.

During linear self-motion the subject travels through space along a straight line to a new location. This is also referred to as “translation” (Andersen, 1986, p. 56; Warren et al., 1988) or “locomotion” (Johansson, 1977; Strelow and Babyn, 1981).

Somatic and vestibular receptors would seem to provide the basis for perception of linear self-motion since it is the muscles, tendons and joints which produce the movement and the vestibular receptors sense the acceleration and deceleration. Despite this, somatic and vestibular sensations are dominated by reliance on visual field motion. This is so robust that illusions of self-motion can be easily induced. Common examples are when the train on the next track begins to move and it is initially perceived as one’s own train moving (or if a large truck begins to move next to one’s car), or when standing close to a large river a perception of self-motion (rather than motion of the river) may occur.

Self-motion illusions, referred to as “linear vection” or “induced translation” (G. J. Andersen, 1986; Bles, 1981), have also been produced in the experimental setting. Lishman and Lee (1973) used a “swinging room” to induce illusions of self-motion and found that “the effects are practically universal” (p. 292). Subjects’ knowledge that they were actually standing on a stable floor and that the “room” was swinging around them did not change the strength of the illusion of self-motion.

When visual field motion is presented only to the periphery of the visual field the illusion of linear self-motion occurs even when accompanied by conflicting vestibular and somatic sensations (Berthoz et al., 1975; Johansson, 1977). This agrees with studies of the effect of visual field motion on the sense of balance when the greatest effect came from peripheral rather than central vision (Amblard and Carblanc, 1980; Lestienne et al., 1977). This same effect has been found in studies of rotary self-motion (see below). Illusions of linear self-motion can also be induced from a radially expanding pattern with an apparent internal depth (eg. from motion parallax and occlusion visual cues) which is presented only to the central visual field (Andersen, 1986, p. 58; Andersen and Braunstein, 1985).

Conversely, if visual field motion is absent (in a dark room) then subjects (incorrectly) perceive that an exterior object is moving rather than (correctly) perceiving their own passive self-motion. Even if somatic and vestibular stimulation are available from repeated accelerations and decelerations (Rock, 1968) or from voluntary jogging (while attempting to stay in place) (Glanzmann, 1987) subjects will usually not perceive their own self-motion if visual field motion is absent.

The direction of linear self-motion can be more accurately performed when visual field motion is available (ie. with a visible background texture rather than darkness or isolated objects in the foreground) (Strelow and Babyn, 1981). Judgements of the heading are more accurate when a high density of visual field texture is available (Warren et al., 1988).

- Sense of rotary self-motion.

The perception of rotary self-motion is closely associated with the vestibular semi-circular canals since these respond to rotational accelerations and decelerations. Nevertheless, even in the absence of vestibular stimulation illusions of rotary self-motion with accompanying nystagmus can be induced from isolated somatic stimulation (Brandt and Buchelle, 1977; Brandt et al., 1977; Lackner and Dizio, 1984), somatic stimulation together with efferent information (Lackner and Dizio, 1984), audio field motion (Dodge, 1923; Lackner, 1977b), or visual field motion (see below). Illusions of rotary self-motion induced by visual field motion are referred to as “induced rotation” or “circular vection” (around the vertical axis), “roll vection” (around the sagittal axis) or “pitch vection” (around the lateral axis) (G. J. Andersen, 1986).

Circular vection is typically induced by rotating a circular wall with a textured surface around a stationary observer. Reducing the luminance levels so that the visual field motion is only perceptible by peripheral vision (Leibowitz et al., 1979), masking the central visual field, or presenting stimuli rotating in the opposite direction in the central visual field, has no effect on the illusion of self-motion, whereas masking peripheral vision eliminates the illusion (Brandt et al., 1973). This type of evidence indicates that peripheral visual field motion is primarily responsible for the perception of rotary self-motion. The importance of peripheral over central vision has also been found in inducing roll vection (Brandt et al., 1975; Held et al., 1975; Reason et al., 1982).

Although illusions of rotary self-motion can be induced by visual field motion alone, when both visual field motion and vestibular stimulation are available the perception of self-motion is quickest and speed estimates are the most accurate (Melchner and Henn, 1981). This indicates how visual and vestibular data function together in the perception of self-motion. Illusions induced from visual field motion are tied to characteristics of the vestibular receptors. With very slow accelerations of the visual field, the self-motion illusion is immediately perceived (Melcher and Henn, 1981). This immediate perception presumably occurs because during slow rotary accelerations very little vestibular stimulation would be expected. However, when the visual field accelerates quickly the self-motion illusion is perceived only gradually, not reaching its full effect until after 30 seconds (Brandt et al., 1973; Wong and Frost, 1978). This latency in the onset of the self-motion illusion presumably occurs because during quick accelerations the vestibular canals would be stimulated during actual rotary accelerations. The illusion of rotary self-motion occurs after the same time that it would take the lymph fluid to stabilise in the vestibular canals during an actual rotation.

The importance of vestibular stimulation in perceptions of rotary self-motion also reveal themselves when illusions of rotary self-motion are induced around a sagittal axis (roll vection). To induce roll vection a subject observes a rotating visual field on a plane parallel to the frontal plane of their body (Held et al., 1975, p. 258). In this case, rather than perceiving a continuous bodily rotation (as in circular vection) the observer perceives that their body is tilted up to a maximum of about 15° (Dichgans et al., 1972; Held et al., 1975). The greater the visual field texture, the greater the illusion of tilt (Brandt et al., 1975; Reason et al., 1982).

Presumably an illusion of a complete 180° roll vection does not occur because during an actual rotation around the sagittal axis (eg. a cartwheel) vestibular otolith stimulation would occur indicating the body’s reorientation relative to gravity. When the same rotating visual-field in the frontal plane is presented to subjects who are lying on their backs, then full 180° roll vection illusion is perceived. In this case the sagittal body axis is oriented along the gravitational vertical and so vestibular otolith stimulation would not be expected during an actual self-motion. Furthermore, when subjects are lying on their backs and the rotating visual field is presented at an angle directly in front of their tilted head, then subjects (incorrectly) perceive that their head is horizontal and their body is tilted. This incorrect perception of head orientation allows the full 180° rotary roll vection illusion to be experienced, presumably because when the head is perceived to be horizontal then there would not be any vestibular otolith sensations expected during an actual rotation (Dizio and Lackner, 1986).

- Circular self-motion.

Locomotion in a curved path can be referred to as circular self-motion and consists of a combination of rotary and linear self-motion. These translation and rotation components must both be distinguished by the perceiver for accurate performance of circular self-motion (Rieger, 1983). As with rotary and linear self-motion, visual field motion is most important for the perception of circular self-motion. When visual field data is not available (eg. a dark room) then circular self-motion will not be perceived even with available vestibular stimulation. Visual field motion alone, or somatic stimulation with efferent knowledge (walking on a circular conveyor belt) are sufficient to elicit illusory perceptions of circular self-motion when the subject actually remains in the same place (ie. no vestibular stimulation). When somatic and efferent data would indicate that the subject was travelling forwards (walking forward on a circular conveyor belt) but contradictory vestibular stimulation would indicate that the subject was travelling backward (the high speed of the conveyor belt caused the subject to actually be travelling backwards) then the vestibular data is ignored and the illusory circular self–motion is perceived in accordance with the somatic and efferent data (Bles, 1981).

Limb Position Sense.

Sensory data from the vision of the body dominates the perception of limb position. Recalling an arm position is more accurate when the arm can be seen than if it can not (Adams et al., 1977; Posner, 1967). Seeing one’s own limbs is the most accurate way of knowing where they are.

A great deal of research has been devoted to discerning the non-visual mechanisms of position sense (for reviews see McCloskey, 1978; Clark and Horch, 1986). Early work recorded discharges from sensory endings in cats’ joint receptors and found that each sensory ending had a maximum response which ranged over a few degrees of joint positions and that these ranges were different for different sensory endings. This was interpreted as indicating that perception of limb position arises solely from joint receptors (Adams et al., 1977, p. 13; Andrew and Dodt, 1953; Gibson, 1966; Roland, 1979; Skoglund, 1956). Even though this notion has been overwhelmingly shown to be erroneous (see below) it is sometimes still adhered to in current texts on dance and exercise (Ellison, 1993, p. 75; Fitt, 1988, p. 266).

In subsequent research joint receptor responses were found to be inadequate for the perception of limb position. Using a different technique for recording joint receptor discharges (for details see McCloskey, 1978, pp. 766-767), Burgess and Clark (1969) found that only 4 out of 278 slowly adapting afferent fibres from the posterior nerve of the cat knee joint were maximally activated at intermediate (rather than extreme) joint angles. In addition, 140 fibres were maximally activated at both full flexion and also full extension of the joint. Clark and Burgess (1975) continued this research and found that only 6 out of 672 fibres tested in the medial nerve, and 45 out of 713 fibres tested in the posterior nerve of the cat knee joint gave slowly adapting responses to intermediate joint angles. Similar results were found in other studies (Clark, 1975; Grigg, 1975). Because joint receptors respond primarily to extreme joint angles, rather than intermediary joint angles, the general conclusion of these findings was that “articular receptors in the knee are not capable of providing appreciable steady-state position information over most of the working range of the joint” (Clark and Burgess, 1975, p. 1462).

Receptors in different joints may have different response characteristics than those in the cat knee joint. For example, nerves for receptors in the cat hip joint have been found to discharge at intermediate joint positions (Carli et al., 1979). Nevertheless, other research findings have shown that anesthetized knee joint capsules in man (Clark et al., 1979) surgical replacement of finger or toe joints with silicone implants (Cross and McCloskey, 1973; Kelso et al., 1980), or deafferentiated joint and skin receptors from a pressure-cuff around the limb (Goodwin et al., 1972a; Roy and Williams, 1979) has no effect on position sense. Therefore, while joint receptors provide some data for position sense their role does not appear to be crucial.

Other research has indicated the role of muscle spindle receptors in the perception of limb position. When the joints, muscles, and skin of the hand are paralysed (by local injection of anaesthesia or by a pressure cuff which cuts off circulation causing total numbness) subjects can still perceive flexion/extension movements and the resultant positions of the fingers, presumably because this perception arises from the long muscles acting on the fingers but which are located in the (non-paralysed) forearm. This perception became even more accurate when the subject lightly tensed the muscles in the forearm (which would increase the data coming from muscular receptors) (Goodwin et al., 1972a; 1972b). The completeness of the anaesthesia within the hand was verified since subjects could not detect lateral finger movements nor could they distinguish between movements at different joints of the same finger. These are movements which are not effected by the long muscles of the forearm, rather, in order to detect or perform these movements, the muscles, skin, or joints within the hand would have to be active (Goodwin et al., 1972b, p. 327).

Further evidence for the role of muscular spindle receptors in the perception of limb positions comes from experiments in which a biceps or triceps tendon is stimulated with a physiotherapy vibrator (placed on the skin above the tendon) which causes a reflex contraction of that muscle (thought to originate from the stimulation of the muscle’s spindle receptors). When the other arm is used to duplicate the perceived motion and position of the vibrated arm (which is hidden from vision), a position illusion (sometimes more than 40°) was evident. The subject perceived the arm position as if the vibrated muscle was stretched longer than it actually was (Goodwin et al., 1972a; 1972c).

If the tonic vibration reflex is allowed to shorten the vibrated muscle then the correct direction of motion will be perceived (viz. elbow flexion if biceps are vibrated, elbow extension if triceps are vibrated) but the distance of movement will be underestimated so that the vibrated muscle is perceived to be stretched longer than it actually is (Goodwin et al. 1972c). If the tonic vibration reflex is not allowed to articulate the elbow (the forearm is restrained by the experimenter or if the subject voluntarily contracts the antagonist muscle) so that an isometric contraction occurs (no change is muscle length), then the elbow will be perceived to be articulating just as if the vibrated muscle was lengthening (Goodwin et al., 1972a; 1972c; McCloskey, 1973).

These position and movement illusions are so robust that even subjects who are informed about the procedure will still perceive the illusions (Goodwin et al., 1972c, p. 1383). This vibration technique can even lead to perceptions of impossible wrist positions, or to perceptions of simultaneous multiple forearms (Craske, 1977).

Using the same vibration technique, McCloskey (1973) separated the illusion of movement from the illusion of position. Velocities of the motion illusion were too fast to have been equated with the size of the position illusion. Longer durations of the vibration caused no change in the position illusion whereas it produced a continual illusion of movement. Loading the muscle (placing a weight on the end of the limb) slowed the velocity of the movement illusion but increased the size of the position illusion. And, with lower frequencies and greater amplitude of vibration the movement illusion was eliminated but the position illusion persisted.

Since muscle spindle primary endings are the most sensitive to vibration it was concluded that these receptors are responsible for the illusions (Goodwin et al., 1972a, p. 744; 1972c, p. 1384). But during lower frequency and greater amplitude vibrations the secondary spindle endings may also play are role in the position and movement illusions (McCloskey, 1973, p. 130).

Further support for the role of muscular receptors in position sense comes from the common finding that arm positions which are actively moved to are recalled better than positions which are imposed by the experimenter onto the subject’s passive arm (Jones, 1972; Kelso, 1977b; Marteniuk, 1973; Paillard and Brouchon, 1968; 1974). When muscles are actively contracting there will be greater sensory discharges from muscle spindle receptors (Matthews, 1933; McCloskey, 1978, p. 770), tendon receptors (Jansen and Rudjord, 1964) and joint receptors (Grigg, 1975; Skoglund, 1956) which should provide more sensory feedback.

This effect of better position recall from active movements also indicates the use of efferent data for deriving the perception of limb position. This is demonstrated when subjects are allowed to actively move their arm to an end-location of their own choosing. In this type of subject-generated movement efferent data would be available and recall of the end-location is most accurate.

Kelso (1977b) distinguishes between factors which may lead to superior memory for self-produced movements: 1) The movement may be actively executed by the subject (active) or the subject’s arm may be passively moved by the experimenter (passive). 2) The end-position of the movement may be chosen by the subject (preselected) or it may be defined by the experimenter with a physical stop on the experimental positioning apparatus (constrained). The combination of active movements to preselected end-locations produces the greatest accuracy. When subjects actively execute preselected end-locations then these can be recalled accurately even with deafferentiated joint and skin receptors in the hand during finger movements (Roy and Williams, 1979). When the active movement is abruptly stopped at an unexpected (constrained) end-location, then this cannot be recalled any better than if the movement was passive (Jones, 1972). A limb position produced by active limb movement can be matched by the opposite limb better than if the position was produced by passive movement (Paillard and Brouchon, 1974). These results indicate that efferent data and muscle spindle receptors are both contributing to the perception and recall of limb positions.

Other studies have also indicated the use of efferent data in limb position sense (eg. Lashley, 1917). Even without any somatic stimulation (when nerves have been severed) after two to six months the vision of the body and efferent data can be sufficient for successful limb movement and positioning in monkeys (eg. climbing up a wire cage or reaching and grasping for food), though this condition does not yield as much accuracy as when somatic stimulation are also available. After more time these monkeys were even able to accomplish the movement task while blindfolded or with the reaching hand out of view (efferent data being the only remaining source of information) (Bossom, 1974; Taub and Berman, 1968).

However, in these deafferentiation studies fine movements such as grasping small objects do not develop to normal accuracy without somatic stimulation (Taub and Berman, 1968; Taub et al., 1973). This indicates that somatic stimulation are necessary for fine positioning and movement.

Skin receptors have also been shown to play a vital role in position sense for certain body areas with a high density of skin receptors. Anesthetized skin around the hands has a detrimental effect on its position accuracy (Moberg, 1983) though anesthetized skin around the knee has no effect (Clark et al., 1979).

Another approach is to suggest that it is not joint angle which is sensed but limb orientation relative to gravity. Soechting (1982) demonstrated that producing an identical forearm orientation was more accurate than producing an identical elbow joint angle. In this approach the pressure sensitivity of joint receptors (Clark, 1975; Clark and Burgess, 1975) could be contributing since the pressure torque in a joint would be in a constant relation with that limb’s orientation to gravity.

Position sense degrades over time. The longer an arm is held in a static position, the less well its position can be matched by the opposite arm (Paillard and Brouchon, 1968; 1974). Presumably this occurs because sensations from quickly adapting receptors are no longer available after a brief time with no movement.

Limb Movement Sense.

The perception of limb movement is tied to the perception of limb position since a position can only be reached by a movement, and every limb movement leads to a new position. This relation is exemplified in the studies of active versus passive produced movements in which the accuracy of body position recall was dependent on the quality of the movement (active vs. passive), with active movement leading to the most accurate position recall (see Longstaff, 1996, Apx. II.43).

However, other evidence reveals that limb movement and limb position are separate. For example, if a very slow speed is used to articulate the knee joint the new position will be perceived but the movement will not (Horch et al., 1975). This leads to the conclusion that perceptions of movement arise from quickly adapting receptors while perceptions of position arise from slowly adapting receptors. The uncorrelated illusions of limb position and limb movement induced by placing a physiotherapy vibrator against the skin over a muscular tendon (see Longstaff, 1996, Apx. 11.43) also indicate that position and movement are separate perceptions (McCloskey, 1973).

Just as with position sense, limb movements can be learned with information from the vision of the body together with efferent knowledge, and eventually with efferent knowledge alone (Bossom, 1974; Taub and Berman, 1968; Longstaff, 1996, Apx. II.43). Vision of the body can also dominate perceptions of limb movement. Subjects can learn a letter-writing task from vision of the body and efferent data with all somatic stimulation eliminated (from a pressure cuff causing total arm numbness) though fine control is best when both vision of the body and somatic stimulation are available (Laszlo and Baker, 1972). A sequence of horizontal linear arm movements was also learned better after one practice trial by simply watching the visual pattern of the movements than by watching the pattern and also bodily performing it (Klein and Posner, 1974). (For discussion of memory and recall characteristics of visual, somatic and audio space, see Longstaff, 1996, Apx. IV.)

Sense of Force; Sense of Exertion.

Perceptions of an object’s weight, or of the amount of force exerted against an object, can be derived from pressure-sensitive skin and joint receptors and tension-sensitive tendon receptors. In certain situations audition of the body would also contribute information about the amount of force which the body has exerted (eg. the sound of the body impacting upon an object). A typical procedure used when estimating an object’s weight is to actively move the object upwards and downwards. This may assist perception since the force required to set the object into motion and then to stop its motion, provides amplified pressure and tension sensations.

The weight of an object is perceived to be heavier when the muscles lifting it are fatigued (McCloskey et al., 1974). Therefore the perception of force appears to be related to the efferent data about the amount of exertion expended. When a reflexive contraction of the muscle is induced (by a physiotherapy vibrator) then subjects can distinguish between the force encountered by the muscle, and the exertion ordered by the motor commands (Ibid). This indicates that the sense of force may be derived by somatic receptors while the sense of exertion is derived from efferent data.


REFERENCES AT:

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