Kinesthesis

Abstract

Kinesthesis is a form of proprioception: the sense of the movement and position of the limbs, generated not by the eyes but by receptors within the muscles, tendons, joints and skin together with signals drawn from the brain's motor commands. Its dominant source is the muscle spindle, whose afferents report how fast and how far a muscle is stretched; vibrating a tendon drives those afferents artificially and produces a compelling illusion of movement, the experiment that settled the spindle's role. Cutaneous receptors and a centrally generated sense of effort contribute alongside it, so that the felt position of a limb is a construction from several signals rather than a read-out of one. This article sets out the muscle-spindle signal, the cutaneous and central contributions, how kinesthetic acuity is measured, and the circuit-level neuroscience now mapping the sense.

Keywords: kinesthesis, proprioception, muscle spindle, movement sense

With the eyes closed, a fingertip brought to the tip of the nose arrives without a glance to guide it. Nothing was seen; yet the brain knew, moment to moment, where the arm was and how fast it was moving. That silent sense is kinesthesis, the perception of limb movement and position, and it runs so smoothly beneath awareness that its existence is easy to miss until a dentist's anaesthetic leaves a numb lip feeling swollen and misplaced, or a tendon buzzed by a vibrator makes a motionless arm feel as though it is swinging away. These failures are the entry point, because kinesthesis — like the other constructed senses — reveals its machinery most clearly when it is fooled (Proske & Gandevia, 2012; Tuthill & Azim, 2018).

What Kinesthesis Is

Kinesthesis is the perception of the movement and the position of the body's own segments — the angle of the elbow, the swing of a stepping leg, the drift of an outstretched hand — sensed from within rather than seen. It is the dynamic, movement-focused aspect of proprioception, the broader sense of the body's configuration in space that Sherrington named when he coined the term in 1906 for the sense by which the body registers its own posture and motion. Where proprioception is often used for the whole family of signals about body state, kinesthesis is reserved for the sense of limb movement and position specifically, and the two words are used almost interchangeably in much of the literature (Proske & Gandevia, 2009).

The percept is not delivered by a single organ. It is assembled from several streams: the muscle spindles that report how long each muscle is and how fast it is changing length, the mechanoreceptors in the skin that deform as a joint moves, the receptors within the joint capsule, and — crucially — signals derived from the motor commands the brain sends to move the limb in the first place. Because these streams can be dissociated experimentally, each pulling the felt position of a limb in a measurable direction, kinesthesis has become a model case for studying how the brain fuses multiple noisy signals into a single coherent percept (Proske & Gandevia, 2012). The modern synthesis treats the muscle spindle as the primary channel while recognising that skin, joint and central signals each add to it, and that their relative weight shifts with the joint, the task and the conditions (Tuthill & Azim, 2018).

The Muscle Spindle and the Sense of Movement

The decisive question for a century was which receptor carries the signal of limb movement, and the answer, established across the 1970s, is the muscle spindle. The spindle is a small encapsulated organ lying in parallel with the muscle fibres; its primary (Ia) afferents fire faster the more the muscle is stretched and, in particular, faster the more quickly it is being stretched, making it a sensor of both muscle length and the velocity of lengthening. The experiment that proved its perceptual role was the tendon-vibration illusion. Goodwin, McCloskey and Matthews applied a vibrator to the tendon of a muscle at the elbow and found that the subject felt the joint move — as though the vibrated muscle were lengthening — even though the arm was held still, and that blocking the joint's own afferents did not abolish the effect. The vibration excites the spindle afferents selectively, and the brain, receiving a lengthening signal, perceives the movement that signal would normally accompany (Goodwin, McCloskey, & Matthews, 1972). Figure 1 shows the arrangement that produces the illusion.

Figure 1

The Tendon-Vibration Illusion of Limb Movement

The illusion is lawful, not merely curious. The illusory velocity of movement rises with the frequency of vibration over the range that the spindle afferents can follow, because each cycle of vibration tends to trigger a spindle discharge, so a higher vibration frequency signals a faster lengthening and therefore a faster felt movement. Matthews drew the general conclusion in his review of the muscular sense: the sense Sherrington had called muscular originates predominantly in the muscle spindles rather than in the joint receptors that an earlier orthodoxy had favoured, with corollary discharges from the motor command contributing a further component (Matthews, 1982). The first demonstration lets the reader apply vibration to a chosen tendon and vary its frequency, watching the illusory limb movement build in the direction and at the speed the spindle signal dictates.

Receptors Beyond the Spindle

The muscle spindle is dominant but not alone. The skin stretches and folds as a joint rotates, and the cutaneous mechanoreceptors that register this deformation supply a movement signal of their own. Collins and colleagues tested this directly by stretching the skin over moving joints and recording both the resulting afferent activity and the perceived movement, and showed that cutaneous input contributes to the sense of movement at the index finger, the elbow and the knee — a genuine kinesthetic signal rather than a mere accompaniment, and one that grows in relative importance at the fingers, where the skin is richly innervated and the muscles that move the digit lie far away in the forearm (Collins, Refshauge, Todd, & Gandevia, 2005). The joint receptors in the capsule, long thought to be the principal movement sensor, in fact contribute most near the extremes of a joint's range, where the capsule is maximally stretched, and comparatively little through the mid-range in which most movement occurs.

The weighting of these sources is not fixed. At a joint well supplied by long muscles, such as the elbow, the spindle signal dominates; at the fingers the cutaneous contribution is proportionally larger; and near the end of the range the joint receptors come into their own. The brain appears to combine the available signals according to how informative each is under the current conditions, which is why cooling or anaesthetising the skin degrades finger kinesthesis more than elbow kinesthesis, and why no single receptor class can be called the organ of the sense (Proske & Gandevia, 2012). This multiplicity is the rule across the proprioceptive senses rather than an exception peculiar to one joint. Table 1 sets out the signals that combine into kinesthesis and the evidence that each contributes.

Central Signals and the Sense of Effort

Kinesthesis draws not only on signals flowing in from the periphery but on signals the brain generates itself. When the motor cortex issues a command to contract a muscle, an internal copy of that command — a corollary discharge, or efference copy — is made available to the perceptual system, and this centrally generated sense of effort contributes to the conscious estimate of where the limb is and how heavy a load it bears. Gandevia and colleagues demonstrated the contribution elegantly by paralysing and anaesthetising a hand so that no movement and no afferent signal were possible, then having the subject attempt to move the now-motionless, insensate hand: the subject experienced an illusory movement of the hand in the direction of the attempted command, a percept that could only have arisen from the motor command itself, since no muscle moved and no afferent fired (Gandevia, Smith, Crawford, Proske, & Taylor, 2006).

That central component explains a family of otherwise puzzling observations. A fatigued muscle requires a larger command to produce the same force, and the limb it moves is felt to be more extended or the load it lifts heavier, because the inflated effort signal is read as a change in position or weight. Lackner showed that proprioceptive signals, when manipulated by vibration, can distort the perceived shape and orientation of the whole body — a vibrated wrist flexor can make the hand feel bent further than any real joint permits, and vibrating the muscles that hold a grasped body part can make that part feel impossibly elongated — demonstrating that the body's felt form is itself a proprioceptive construction open to systematic distortion (Lackner, 1988). The second demonstration contrasts the two contributions directly, letting the reader match the felt position of one arm with the other and then add a fatiguing load to watch the effort signal bias the match.

Measuring Kinesthetic Acuity

Because kinesthesis is invisible, measuring it requires tasks that externalise the internal sense. Two families dominate. In a joint-position-matching task the experimenter places one limb at a target angle and the subject attempts to reproduce that angle with the same or the opposite limb; the difference between the target and the reproduction, the matching error, indexes position sense. In a threshold-to-detection-of-passive-movement task the limb is moved slowly by a motor and the subject signals the instant movement is felt; the excursion needed before detection indexes movement sense. Goble reviewed the joint-position-matching method and its migration from the laboratory into clinical practice, noting that ipsilateral and contralateral matching probe partly different things and that the method's apparent simplicity conceals choices — active versus passive positioning, the limb used to indicate — that materially change the score (Goble, 2010).

The movement-detection threshold is lawfully related to the velocity of the imposed movement: the more slowly a joint is moved, the larger the angular excursion required before the movement is detected, because the spindle's velocity-sensitive signal is weaker at low speeds. Thresholds are smallest at the proximal joints and larger at the distal ones, and they rise with age and with injury, which is what makes them clinically useful. Han and colleagues reviewed the proliferation of proprioception assessment methods across sport and rehabilitation science and argued for matching the method to the question, since position-matching, movement-detection and active-movement-reproduction tasks correlate only moderately and so are not interchangeable measures of one underlying acuity (Han, Waddington, Adams, Anson, & Liu, 2016). The third demonstration runs a movement-detection task, letting the reader set the movement velocity and read off the detection threshold the velocity dependence predicts.

Worked Example

The two quantitative facts of kinesthesis become concrete when the numbers are worked, and the demonstrations reproduce this arithmetic. Take the vibration illusion first. The spindle primary afferent tends to fire one impulse per cycle of tendon vibration up to a ceiling, so the extra afferent rate the vibration adds is approximately the vibration frequency itself. If the brain reads a given afferent rate as a given lengthening velocity, then the illusory velocity of movement should rise roughly in proportion to vibration frequency over the range the afferent can follow. Doubling the vibration from 40 to 80 hertz therefore roughly doubles the felt speed of the illusory movement, and the illusion grows weak above the frequency at which the afferent can no longer lock one spike to each cycle, typically around 80 to 100 hertz — exactly the saturating rise the demonstration plots.

Now the movement-detection threshold. Because the spindle reports the velocity of stretch, a slower movement produces a weaker afferent signal, so the joint must rotate through a larger angle before the movement is felt. A simple model captures the dependence: the detection threshold in degrees is a small irreducible floor plus a term inversely proportional to velocity, threshold = 0.3 + 0.8 / v, with v in degrees per second. At an imposed velocity of 4 degrees per second the threshold is 0.3 + 0.8 / 4 = 0.5 degrees; at 1 degree per second it is 0.3 + 0.8 / 1 = 1.1 degrees; and at 0.5 degrees per second it rises to 0.3 + 0.8 / 0.5 = 1.9 degrees. Halving the velocity raises the angular threshold, which is why clinicians test movement sense with slow, controlled displacements: the slow movement is the harder test, and a degraded sense fails it first — exactly the curve the demonstration plots.

Discussion

Kinesthesis began the twentieth century as a puzzle about which receptor carried the signal and ends it as a worked example of multisensory construction. The muscle spindle is the primary channel, proven by the vibration illusion and confirmed by the recordings that followed, but it is not the whole story: cutaneous and joint receptors add their own movement signals, weighted by joint and condition, and the motor command itself contributes a central sense of effort that shapes the felt position of a limb (Goodwin, McCloskey, & Matthews, 1972; Collins, Refshauge, Todd, & Gandevia, 2005; Gandevia, Smith, Crawford, Proske, & Taylor, 2006). That the felt shape of the whole body can be distorted by vibrating a single muscle shows how thoroughly the body schema rests on this sense (Lackner, 1988).

The practical payoff is measurement. Because kinesthetic acuity declines with age, injury and disease and can be rebuilt by training, quantifying it matters for rehabilitation and sport, and the field's progress has depended on recognising that position-matching and movement-detection tasks are not one measure but several (Goble, 2010; Han, Waddington, Adams, Anson, & Liu, 2016). The synthesis that Proske and Gandevia assembled across their reviews — the spindle primary, the others contributory, the central signal real — now frames the sense, and the questions that remain are increasingly about mechanism at the level of the neural circuit rather than about which organ matters (Proske & Gandevia, 2012; Proske & Gandevia, 2018).

Current Directions

The open frontier in kinesthesis is the circuit. For most of its history the field worked from the receptor and the percept inward and outward respectively, with the central processing between them largely a black box; the contemporary program, surveyed by Tuthill and Azim, is to map the proprioceptive pathway neuron by neuron — the molecularly defined classes of sensory neuron that innervate the spindle, the spinal and brainstem relays that process their signals, and the ascending routes to cortex — using the genetic tools of the mouse and the fly to label and manipulate each element (Tuthill & Azim, 2018). The promise is a mechanistic account of how the velocity and length signals the spindle reports are transformed into the coherent sense of a moving limb, and of how the central motor signal is combined with them.

This circuit-level work converges with a renewed interest in proprioceptive signals for the control of prosthetic and robotic limbs, where restoring a sense of movement to an artificial hand requires knowing precisely which afferent signals the brain reads as movement and how they are weighted — the same cutaneous, spindle and central contributions the behavioural work identified, now posed as an engineering specification. Proske and Gandevia's most recent synthesis frames the kinesthetic senses for this next phase, carrying the behavioural and physiological consensus into the era of circuit neuroscience and neural interfaces (Proske & Gandevia, 2018).

Common Misconceptions

The joints sense limb position; muscles only produce movement.

This was the orthodoxy until the 1970s and it is wrong. The muscle spindle is the dominant sensor of limb movement and position; the joint receptors contribute chiefly near the extremes of the range, and vibrating a muscle tendon — not a joint — is what produces the illusion of movement (Goodwin, McCloskey, & Matthews, 1972; Matthews, 1982).

Kinesthesis is just incoming information from the body's receptors.

A copy of the outgoing motor command contributes too. A paralysed, anaesthetised hand that cannot move and sends no afferent signal is still felt to move when the subject tries to move it, a percept that can only come from the motor command — so the sense draws on central as well as peripheral signals (Gandevia, Smith, Crawford, Proske, & Taylor, 2006).

Kinesthesis and proprioception are different senses.

They are not cleanly separable. Kinesthesis is the movement-and-position component of proprioception, the broader sense of body state; the terms are used almost interchangeably, with kinesthesis emphasising the sense of limb movement specifically (Proske & Gandevia, 2009).

Glossary

Corollary discharge.

An internal copy of a motor command made available to perceptual systems; also called efference copy, it supplies the central sense of effort that contributes to kinesthesis.

Cutaneous mechanoreceptor.

A receptor in the skin that responds to stretch and deformation; as the skin folds around a moving joint these receptors supply a kinesthetic signal, especially at the fingers.

Efference copy.

See corollary discharge: a copy of the outgoing motor command used by the brain to anticipate and interpret the sensory consequences of its own movements.

Joint position matching.

A task measuring position sense in which a limb is placed at a target angle and the subject reproduces that angle with the same or the opposite limb; the reproduction error is the score.

Joint receptor.

A mechanoreceptor in the joint capsule signalling joint angle; once thought the principal movement sensor, it contributes chiefly near the extremes of a joint's range rather than through the mid-range.

Kinesthesis.

The sense of the movement and position of the limbs, generated from muscle, joint and skin receptors and from central motor signals; the movement-focused component of proprioception.

Movement-detection threshold.

The smallest angular excursion of a passively moved joint that can be detected; it grows as the movement velocity falls, because the spindle's signal is velocity-sensitive.

Muscle spindle.

An encapsulated stretch receptor lying in parallel with the muscle fibres; its primary (Ia) afferents signal muscle length and the velocity of lengthening and are the dominant source of kinesthesis.

Position sense.

The static component of kinesthesis: the sense of the steady angle at which a joint is held, measured by joint-position-matching tasks and distinct from the sense of ongoing movement.

Primary (Ia) afferent.

The fast sensory fibre from a muscle spindle that is especially sensitive to the rate of muscle stretch; the fibre excited by tendon vibration.

Proprioception.

The broad sense of the body's position, movement and force, comprising kinesthesis together with the senses of static limb position and of muscular effort.

Sense of effort.

The centrally generated feeling of exertion accompanying a motor command; inflated by fatigue, it biases the felt position of a limb and the felt heaviness of a load.

Tendon vibration illusion.

The illusory sense of limb movement produced when a vibrator applied to a muscle's tendon excites its spindle afferents, signalling a lengthening that the brain reads as motion.

Velocity sensitivity.

The property of the spindle primary afferent whereby its firing rate rises with the speed of muscle stretch, which makes slow joint movements harder to detect than fast ones.

Key Researchers

Simon C. Gandevia

. Neuroscience Research Australia (NeuRA) and UNSW Sydney; a human motor physiologist whose experiments dissected the contributions to position sense of muscle afferents, skin and centrally generated motor commands, showing that an efference-copy signal contributes to the conscious sense of limb position. Faculty Page - Wikipedia - Wikidata

Jia Han

. Shanghai University of Medicine and Health Sciences; Adjunct Professor at the University of Canberra, he works on the measurement of proprioception and kinesthetic acuity, including the critical review of assessment methods that frames how movement and position sense are quantified in sport and rehabilitation science. ORCID - Google Scholar

Peter B. C. Matthews

(1928-2020). University of Oxford; he established the muscle spindle as the primary signal for kinesthesis, his vibration-illusion experiments and his review of the muscular sense showing that spindle afferents, not joint receptors, carry the dominant signal of limb movement and position. Wikipedia - Wikidata

Uwe Proske

. Monash University (Emeritus Professor of Physiology); co-author of the definitive modern reviews of the kinesthetic and proprioceptive senses, synthesising the muscle-spindle, cutaneous and corollary-discharge contributions to the sense of limb position and movement. Faculty Page

Charles Scott Sherrington

(1857-1952). University of Oxford; he coined the term proprioception in 1906 for the sense by which the body registers its own movement and position, and his account of the proprioceptive system is the conceptual root of the modern study of kinesthesis. Nobel laureate in Physiology or Medicine (1932). Wikipedia - Wikidata

Janet L. Taylor

. Neuroscience Research Australia (NeuRA) and Edith Cowan University; a human motor physiologist and co-author of the work showing that motor commands contribute to position sense, clarifying how central signals and muscle fatigue shape the perception of limb position and effort. Faculty Page - Google Scholar

John C. Tuthill

. University of Washington (Department of Physiology and Biophysics); he leads contemporary circuit-level work on proprioception, mapping the sensory neurons and central pathways that encode body movement across model and mammalian systems, and his primer frames the modern neuroscience of the sense. ORCID - Faculty Page - Google Scholar

Frequently Asked Questions

What is kinesthesis?

Kinesthesis is the sense of the movement and position of the limbs: knowing where the arm is and how fast it is moving without looking. It is the movement-focused component of proprioception, generated by receptors in the muscles, joints and skin together with signals derived from the brain's own motor commands (Proske & Gandevia, 2009).

How is kinesthesis different from proprioception?

Kinesthesis is one part of proprioception. Proprioception is the broad sense of the body's position, movement and force; kinesthesis refers specifically to the sense of limb movement and position. The two terms overlap heavily and are often used interchangeably (Proske & Gandevia, 2012).

Which receptor is most important for kinesthesis?

The muscle spindle. Its primary afferents report muscle length and the velocity of lengthening, and vibrating a tendon to excite them produces a vivid illusion of limb movement, which proved that the spindle, not the joint receptor, is the dominant movement sensor (Goodwin, McCloskey, & Matthews, 1972; Matthews, 1982).

What is the tendon vibration illusion?

When a vibrator is applied to a muscle's tendon, it excites the muscle's spindle afferents as though the muscle were lengthening, and the brain perceives a movement of the joint that is not actually happening. The illusory speed rises with the vibration frequency, demonstrating the spindle's role in sensing movement (Goodwin, McCloskey, & Matthews, 1972).

Do the skin and joints contribute to kinesthesis?

Yes. Cutaneous receptors that register the stretching of skin around a moving joint contribute a genuine movement signal, especially at the fingers, and joint receptors contribute most near the extremes of a joint's range. The muscle spindle remains dominant through the mid-range of most joints (Collins, Refshauge, Todd, & Gandevia, 2005).

Does the brain's own motor command contribute to the sense?

Yes. A copy of the outgoing motor command, a corollary discharge, produces a sense of effort that contributes to felt limb position. A paralysed, anaesthetised hand is still felt to move when the subject tries to move it, a percept that can only come from the command itself (Gandevia, Smith, Crawford, Proske, & Taylor, 2006).

How is kinesthetic acuity measured?

Chiefly by two kinds of task: joint-position matching, in which a limb is placed at an angle and the subject reproduces it, and movement detection, in which the subject signals when a slowly imposed movement is first felt. The tasks measure partly different things and are not interchangeable (Goble, 2010; Han, Waddington, Adams, Anson, & Liu, 2016).

Why are slow movements harder to detect than fast ones?

Because the muscle spindle signals the velocity of stretch: a slow movement produces a weaker afferent signal, so the joint must rotate through a larger angle before the movement is detected. This is why clinical tests of movement sense use slow, controlled displacements (Proske & Gandevia, 2012).

References