Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Kinesthetic Senses

Uwe Proske, Simon C. Gandevia

10.1002/cphy.c170036

Source: Volume 8, Issue 3, July 2018

Published online: June 2018

Full Article on Wiley Online Library



ABSTRACT

The kinesthetic senses are the senses of position and movement of the body, senses we are aware of only on introspection. A method used to study kinesthesia is muscle vibration, which engages afferents of muscle spindles to trigger illusions of movement and changed position. When vibrating elbow flexors, it generates sensations of forearm extension, when vibrating extensors, sensations of forearm flexion. Vibrating the elbow joint produces no illusion. Vibrating flexors and extensors together at the same frequency also produces no illusion, because what is perceived is the signal difference between antagonist muscles of each arm and between arms. The size of the illusion depends on how the muscle has been conditioned beforehand, due to a property of muscle called thixotropy. When measuring the illusion, blindfolded subjects may carry out a matching or pointing task. In pointing, signals from muscle spindles are less important than in matching. Afferent signals from kinesthetic receptors project to areas of somatosensory cortex to generate sensations of detection and location. This is referred to the body model, which provides information about size and shape of body parts. Kinesthesia, together with vision and touch, is associated with the sense of body ownership. All three can combine or each, on its own, can generate ownership. Related is the sense of agency, the sense of being responsible for one's own actions. In recent times, much progress has been made using neuroimaging techniques to identify the various areas of the brain likely to be responsible for generating these sensations. © 2017 American Physiological Society. Compr Physiol 8:1157‐1183, 2018.

Comprehensive Physiology offers downloadable PowerPoint presentations of figures for non-profit, educational use, provided the content is not modified and full credit is given to the author and publication.

Download a PowerPoint presentation of all images


Figure 1. Figure 1. Muscle thixotropy. (A) Diagrammatic representation of a string of passive sarcomeres, part of a myofibril, containing thick and thin myofilaments. Scattered randomly along the length of the myofibril are occasional points of attachment between thick and thin filaments, the stable cross‐bridges (red circles). They are responsible for giving muscle its thixotropic property. (B) Tension changes in a passive muscle during ramp stretch and shortening. During stretch, due to the presence of attached cross‐bridges, tension rises steeply, to plateau out as the yield point is reached, and bridges begin to detach to reform at the longer length. During shortening, attached cross‐bridges exert a splinting effect on the shortening muscle, leading tension to fall steeply and remain low for the remainder of the shortening. Length and tension traces redrawn, with permission, from Hill (83).
Figure 2. Figure 2. (A) Flexion conditioning of elbow muscles: The blindfolded subject flexes their arm so that the paddle supporting the forearm is at right angles to the supporting base (conditioning angle). The experimenter holds the paddle in position while the subject contracts their elbow flexors, trying to pull the paddle toward their body. After a brief, half‐maximum voluntary contraction, the subject relaxes their arm and the experimenter moves it to the test position (actual). This is perceived as more extended than the true position, as shown by the image ghost (perceived angle). (B) Extension conditioning of elbow muscles: The blindfolded subject extends their forearm to lie on the supporting base (conditioning angle). They then push down on the base, to contract their elbow extensors. After a half‐maximal contraction, the subject relaxes their arm and the experimenter moves it to the test angle (actual). This is perceived as more flexed than the true position, as shown by the image ghost (perceived angle).
Figure 3. Figure 3. Distribution of position errors at the forearm from different forms of thixotropic conditioning: The blindfolded subjects matched positions of their forearms after conditioning of elbow muscles. Left‐hand values: mean (±SEM) position errors for 14 subjects at 5 s after arm alignment. After flexion conditioning of both arms, small errors in the direction of flexion are made (blue circle); after extension conditioning, similar sized errors are made in the direction of extension (red circle). Replotted, with permission, from Ref. (162). Middle values: position errors for the same 14 subjects after co‐conditioning of the reference arm (see Fig. 4) and flexion conditioning of the indicator arm (blue circle) or extension conditioning of the indicator arm (red circle). Large errors in the direction of flexion are made after flexion conditioning of the indicator arm and in the direction of extension after extension conditioning of the indicator arm. Data replotted, with permission, from Ref (162). Right‐hand values: errors (±SEM) for nine subjects after co‐conditioning of the reference arm with slack introduced in the indicator arm. Slack is introduced in one of two ways; the indicator is flexion conditioned and then the arm is moved into full extension before being returned to the test angle (blue circle). Alternatively, the arm is extension conditioned, then fully flexed before being returned to the test angle (red circle). Data replotted, with permission, from Ref. (161).
Figure 4. Figure 4. Test angle co‐conditioning: The experimenter moves the blindfolded subject's forearm to the test position (actual). While holding the paddle, the experimenter asks the subject first to pull it toward their body, to generate a contraction in elbow flexors, then to push it into extension to contract elbow extensors. The subject then relaxes their arm, which is perceived to adopt a position close to its true position, as shown by the ghost image (perceived angle).
Figure 5. Figure 5. Measuring position sense in matching and pointing tasks: In the matching task (A), blindfolded subjects’ arms were strapped to paddles, one arm designated the reference, the other the indicator. Forearm position was measured by potentiometers located at the hinges of the paddles, which were colinear with the elbow joint. The experimenter placed the reference arm at a test angle and the subject held it there while they moved their indicator arm into a matching position. In the pointing task (B), the two arms were separated by a screen (dashed line) which blocked the subject's view of the reference arm. The reference arm was strapped to a paddle, as before, and was placed at the test angle by the experimenter. Once the reference arm was in position, the subject pressed a lever with their other hand to move the pointer paddle to align it with the perceived position of the hidden reference arm. Data replotted, with permission, from Ref. (163).
Figure 6. Figure 6. Position errors in matching and pointing tasks. (A) Two arm matching task. Left‐hand data points, both arms were flexion conditioned before the match; red circle, mean (±SEM) error for 14 subjects, blue circle, predicted error. Right‐hand data points, the arms were extension conditioned; red circle, mean measured error, blue circle, expected error. Replotted, with permission, from Ref. (163). (B) Pointing to the position of a hidden arm. Left‐hand data points, the arm was flexion conditioned. Red circle, mean (±SEM) error for 14 subjects, blue circle, expected error. Right‐hand values, the arm was extension conditioned. Red circle, observed error, blue circle, expected error. Replotted, with permission, from Ref. (163).
Figure 7. Figure 7. Subjects have their right hand resting on the lower table. The right (test) index finger is held in a pipe connected to a shaft on which an artificial prosthetic finger is mounted. 12 cm separates the subject's test index and the artificial finger. The vertical dotted line indicates the axis of rotation of the shaft, which was colinear with the proximal interphalangeal joint of the artificial finger and the subject's test finger. A coupling on the shaft allowed movement between the artificial finger and the subject's test finger to be either congruent or incongruent. In some studies, vision is excluded and the experimenter holds the thumb in a passive pinch grip on the artificial finger. In other studies, the experimenter moves the artificial finger and this can be seen by the subject (the left hand is not involved). Redrawn, with permission, from Ref. (82).
Figure 8. Figure 8. (A) The effect of congruent movement and blocking the digital nerves of the grasping and test fingers on perceived ownership over the artificial finger. The median ± interquartile range responses to the statement “I feel that I am holding my right index finger with my left hand.” Following the digital nerve blocks median responses were higher after congruent movement than incongruent movement. (B) Perceived vertical spacing between the index fingers for congruent and incongruent movement trials after the digital nerves of the test index finger and the grasping index finger and thumb were blocked with local anesthetic. A smaller median perceived spacing was reported after congruent movement compared to incongruent movement. Results show median ± interquartile range. Replotted, with permission, from Ref. (24).


Figure 1. Muscle thixotropy. (A) Diagrammatic representation of a string of passive sarcomeres, part of a myofibril, containing thick and thin myofilaments. Scattered randomly along the length of the myofibril are occasional points of attachment between thick and thin filaments, the stable cross‐bridges (red circles). They are responsible for giving muscle its thixotropic property. (B) Tension changes in a passive muscle during ramp stretch and shortening. During stretch, due to the presence of attached cross‐bridges, tension rises steeply, to plateau out as the yield point is reached, and bridges begin to detach to reform at the longer length. During shortening, attached cross‐bridges exert a splinting effect on the shortening muscle, leading tension to fall steeply and remain low for the remainder of the shortening. Length and tension traces redrawn, with permission, from Hill (83).


Figure 2. (A) Flexion conditioning of elbow muscles: The blindfolded subject flexes their arm so that the paddle supporting the forearm is at right angles to the supporting base (conditioning angle). The experimenter holds the paddle in position while the subject contracts their elbow flexors, trying to pull the paddle toward their body. After a brief, half‐maximum voluntary contraction, the subject relaxes their arm and the experimenter moves it to the test position (actual). This is perceived as more extended than the true position, as shown by the image ghost (perceived angle). (B) Extension conditioning of elbow muscles: The blindfolded subject extends their forearm to lie on the supporting base (conditioning angle). They then push down on the base, to contract their elbow extensors. After a half‐maximal contraction, the subject relaxes their arm and the experimenter moves it to the test angle (actual). This is perceived as more flexed than the true position, as shown by the image ghost (perceived angle).


Figure 3. Distribution of position errors at the forearm from different forms of thixotropic conditioning: The blindfolded subjects matched positions of their forearms after conditioning of elbow muscles. Left‐hand values: mean (±SEM) position errors for 14 subjects at 5 s after arm alignment. After flexion conditioning of both arms, small errors in the direction of flexion are made (blue circle); after extension conditioning, similar sized errors are made in the direction of extension (red circle). Replotted, with permission, from Ref. (162). Middle values: position errors for the same 14 subjects after co‐conditioning of the reference arm (see Fig. 4) and flexion conditioning of the indicator arm (blue circle) or extension conditioning of the indicator arm (red circle). Large errors in the direction of flexion are made after flexion conditioning of the indicator arm and in the direction of extension after extension conditioning of the indicator arm. Data replotted, with permission, from Ref (162). Right‐hand values: errors (±SEM) for nine subjects after co‐conditioning of the reference arm with slack introduced in the indicator arm. Slack is introduced in one of two ways; the indicator is flexion conditioned and then the arm is moved into full extension before being returned to the test angle (blue circle). Alternatively, the arm is extension conditioned, then fully flexed before being returned to the test angle (red circle). Data replotted, with permission, from Ref. (161).


Figure 4. Test angle co‐conditioning: The experimenter moves the blindfolded subject's forearm to the test position (actual). While holding the paddle, the experimenter asks the subject first to pull it toward their body, to generate a contraction in elbow flexors, then to push it into extension to contract elbow extensors. The subject then relaxes their arm, which is perceived to adopt a position close to its true position, as shown by the ghost image (perceived angle).


Figure 5. Measuring position sense in matching and pointing tasks: In the matching task (A), blindfolded subjects’ arms were strapped to paddles, one arm designated the reference, the other the indicator. Forearm position was measured by potentiometers located at the hinges of the paddles, which were colinear with the elbow joint. The experimenter placed the reference arm at a test angle and the subject held it there while they moved their indicator arm into a matching position. In the pointing task (B), the two arms were separated by a screen (dashed line) which blocked the subject's view of the reference arm. The reference arm was strapped to a paddle, as before, and was placed at the test angle by the experimenter. Once the reference arm was in position, the subject pressed a lever with their other hand to move the pointer paddle to align it with the perceived position of the hidden reference arm. Data replotted, with permission, from Ref. (163).


Figure 6. Position errors in matching and pointing tasks. (A) Two arm matching task. Left‐hand data points, both arms were flexion conditioned before the match; red circle, mean (±SEM) error for 14 subjects, blue circle, predicted error. Right‐hand data points, the arms were extension conditioned; red circle, mean measured error, blue circle, expected error. Replotted, with permission, from Ref. (163). (B) Pointing to the position of a hidden arm. Left‐hand data points, the arm was flexion conditioned. Red circle, mean (±SEM) error for 14 subjects, blue circle, expected error. Right‐hand values, the arm was extension conditioned. Red circle, observed error, blue circle, expected error. Replotted, with permission, from Ref. (163).


Figure 7. Subjects have their right hand resting on the lower table. The right (test) index finger is held in a pipe connected to a shaft on which an artificial prosthetic finger is mounted. 12 cm separates the subject's test index and the artificial finger. The vertical dotted line indicates the axis of rotation of the shaft, which was colinear with the proximal interphalangeal joint of the artificial finger and the subject's test finger. A coupling on the shaft allowed movement between the artificial finger and the subject's test finger to be either congruent or incongruent. In some studies, vision is excluded and the experimenter holds the thumb in a passive pinch grip on the artificial finger. In other studies, the experimenter moves the artificial finger and this can be seen by the subject (the left hand is not involved). Redrawn, with permission, from Ref. (82).


Figure 8. (A) The effect of congruent movement and blocking the digital nerves of the grasping and test fingers on perceived ownership over the artificial finger. The median ± interquartile range responses to the statement “I feel that I am holding my right index finger with my left hand.” Following the digital nerve blocks median responses were higher after congruent movement than incongruent movement. (B) Perceived vertical spacing between the index fingers for congruent and incongruent movement trials after the digital nerves of the test index finger and the grasping index finger and thumb were blocked with local anesthetic. A smaller median perceived spacing was reported after congruent movement compared to incongruent movement. Results show median ± interquartile range. Replotted, with permission, from Ref. (24).
References
 1.Abdulkarim Z, Ehrsson HH. No causal link between changes in hand position sense and feeling of limb ownership in the rubber hand illusion. Atten Percept Psychophys 78: 707‐720, 2016.
 2.Albert F, Bergenheim M, Ribot‐Ciscar E, Roll JP. The Ia afferent feedback of a given movement evokes the illusion of the same movement when returned to the subject via muscle tendon vibration. Exp Brain Res 172: 163‐174, 2006.
 3.Allen TJ, Ansems GE, Proske U. Effects of muscle conditioning on position sense at the human forearm during loading or fatigue of elbow flexors and the role of the sense of effort. J Physiol 580: 423‐434, 2007.
 4.Allen TJ, Leung M, Proske U. The effect of fatigue from exercise on human limb position sense. J Physiol 588: 1369‐1377, 2010.
 5.Ansems GE, Allen TJ, Proske U. Position sense at the human forearm in the horizontal plane during loading and vibration of elbow muscles. J Physiol 576: 445‐455, 2006.
 6.Banks RW. An allometric analysis of the number of muscle spindles in mammalian skeletal muscles. J Anat 208: 753‐768, 2006.
 7.Bastian H. The “muscular sense”; its nature and localization. Brain 10: 1‐36, 1888.
 8.Bellan V, Wallwork SB, Stanton TR, Reverberi C, Gallace A, Moseley GL. No telescoping effect with dual tendon vibration. PLoS One 11: e0157351, 2016.
 9.Bergenheim M, Ribot‐Ciscar E, Roll JP. Proprioceptive population coding of two‐dimensional limb movements in humans: I. Muscle spindle feedback during spatially oriented movements. Exp Brain Res 134: 301‐310, 2000.
 10.Berlucchi G, Aglioti SM. The body in the brain revisited. Exp Brain Res 200: 25‐35, 2010.
 11.Bewick GS, Banks RW. Mechanotransduction in the muscle spindle. Pflugers Arch 467: 175‐190, 2015.
 12.Bock O, Pipereit K, Mierau A. A method to reversibly degrade proprioceptive feedback in research on human motor control. J Neurosci Methods 160: 246‐250, 2007.
 13.Bosco G, Poppele RE. Reference frames for spinal proprioception: Kinematics based or kinetics based? J Neurophysiol 83: 2946‐2955, 2000.
 14.Botvinick M, Cohen J. Rubber hands ‘feel’ touch that eyes see. Nature 391: 756, 1998.
 15.Bowering KJ, O'Connell NE, Tabor A, Catley MJ, Leake HB, Moseley GL, Stanton TR. The effects of graded motor imagery and its components on chronic pain: A systematic review and meta‐analysis. J Pain 14: 3‐13, 2013.
 16.Brecht M. The body model theory of somatosensory cortex. Neuron 94: 985‐992, 2017.
 17.Brown LE, Rosenbaum DA, Sainburg RL. Limb position drift: implications for control of posture and movement. J Neurophysiol 90: 3105‐3118, 2003.
 18.Brown MC, Enberg I, Matthews PB. The relative sensitivity to vibration of muscle receptors of the cat. J Physiol 192: 773‐800, 1967.
 19.Brun C, Guerraz M. Anchoring the “floating arm”: Use of proprioceptive and mirror visual feedback from one arm to control involuntary displacement of the other arm. Neuroscience 310: 268‐278, 2015.
 20.Burgess PR, Clark FJ. Characteristics of knee joint receptors in the cat. J Physiol 203: 317‐335, 1969.
 21.Burgess PR, Wei JY, Clark FJ, Simon J. Signaling of kinesthetic information by peripheral sensory receptors. Annu Rev Neurosci 5: 171‐187, 1982.
 22.Burke D, Gandevia SC, Macefield G. Responses to passive movement of receptors in joint, skin and muscle of the human hand. J Physiol 402: 347‐361, 1988.
 23.Burke D, Hagbarth KE, Skuse NF. Voluntary activation of spindle endings in human muscles temporarily paralysed by nerve pressure. J Physiol 287: 329‐336, 1979.
 24.Butler AA, Héroux ME, Gandevia SC. Body ownership and a new proprioceptive role for muscle spindles. Acta Physiol 220: 19‐27, 2017.
 25.Capaday C, Cooke JD. Vibration‐induced changes in movement‐related EMG activity in humans. Exp Brain Res 52: 139‐146, 1983.
 26.Cardinali L, Frassinetti F, Brozzoli C, Urquizar C, Roy AC, Farne A. Tool‐use induces morphological updating of the body schema. Curr Biol 19: R478‐R479, 2009.
 27.Chancel M, Blanchard C, Guerraz M, Montagnini A, Kavounoudias A. Optimal visuotactile integration for velocity discrimination of self‐hand movements. J Neurophysiol 116: 1522‐1535, 2016.
 28.Chowdhury RH, Tresch MC, Miller LE. Musculoskeletal geometry accounts for apparent extrinsic representation of paw position in dorsal spinocerebellar tract. J Neurophysiol 118: 234‐242, 2017.
 29.Clark FJ, Burgess RC, Chapin JW, Lipscomb WT. Role of intramuscular receptors in the awareness of limb position. J Neurophysiol 54: 1529‐1540, 1985.
 30.Clark FJ, Grigg P, Chapin JW. The contribution of articular receptors to proprioception with the fingers in humans. J Neurophysiol 61: 186‐193, 1989.
 31.Cobo JL, Abbate F, de Vicente JC, Cobo J, Vega JA. Searching for proprioceptors in human facial muscles. Neurosci Lett 640: 1‐5, 2017.
 32.Cole J. Losing Touch: A Man Without His Body. Oxford: Oxford University Press, 2016.
 33.Collins DF, Prochazka A. Movement illusions evoked by ensemble cutaneous input from the dorsum of the human hand. J Physiol 496(Pt 3): 857‐871, 1996.
 34.Collins DF, Refshauge KM, Todd G, Gandevia SC. Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. J Neurophysiol 94: 1699‐1706, 2005.
 35.Cordo P, Gandevia SC, Hales JP, Burke D, Laird G. Force and displacement‐controlled tendon vibration in humans. Electroencephalogr Clin Neurophysiol 89: 45‐53, 1993.
 36.Cordo P, Gurfinkel VS, Bevan L, Kerr GK. Proprioceptive consequences of tendon vibration during movement. J Neurophysiol 74: 1675‐1688, 1995.
 37.Craske B. Perception of impossible limb positions induced by tendon vibration. Science 196: 71‐73, 1977.
 38.Crowe A, Matthews PB. The effects of stimulation of static and dynamic fusimotor fibres on the response to stretching of the primary endings of muscle spindles. J Physiol 174: 109‐131, 1964.
 39.de Vignemont F. Body schema and body image–‐pros and cons. Neuropsychologia 48: 669‐680, 2010.
 40.Dimitriou M. Enhanced muscle afferent signals during motor learning in humans. Curr Biol 26: 1062‐1068, 2016.
 41.Dummer T, Picot‐Annand A, Neal T, Moore C. Movement and the rubber hand illusion. Perception 38: 271‐280, 2009.
 42.Edin BB. Finger joint movement sensitivity of non‐cutaneous mechanoreceptor afferents in the human radial nerve. Exp Brain Res 82: 417‐422, 1990.
 43.Ehrsson HH, Holmes NP, Passingham RE. Touching a rubber hand: Feeling of body ownership is associated with activity in multisensory brain areas. J Neurosci 25: 10564‐10573, 2005.
 44.Ettlinger G, Kalsbeck JE. Changes in tactile discrimination and in visual reaching after successive and simultaneous bilateral posterior parietal ablations in the monkey. J Neurol Neurosurg Psychiatry 25: 256‐268, 1962.
 45.Feinberg TE, Venneri A, Simone AM, Fan Y, Northoff G. The neuroanatomy of asomatognosia and somatoparaphrenia. J Neurol Neurosurg Psychiatry 81: 276‐281, 2010.
 46.Ferrell WR. The effect of acute joint distension on mechanoreceptor discharge in the knee of the cat. Q J Exp Physiol 72: 493‐499, 1987.
 47.Ferrell WR, Smith A. The effect of digital nerve block on position sense at the proximal interphalangeal joint of the human index finger. Brain Res 425: 369‐371, 1987.
 48.Flor H, Elbert T, Knecht S, Wienbruch C, Pantev C, Birbaumer N, Larbig W, Taub E. Phantom‐limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 375: 482‐484, 1995.
 49.Flor H, Nikolajsen L, Staehelin Jensen T. Phantom limb pain: A case of maladaptive CNS plasticity? Nat Rev Neurosci 7: 873‐881, 2006.
 50.Fontan A, Cignetti F, Nazarian B, Anton JL, Vaugoyeau M, Assaiante C. How does the body representation system develop in the human brain? Dev Cogn Neurosci 24: 118‐128, 2017.
 51.Frith CD, Blakemore SJ, Wolpert DM. Abnormalities in the awareness and control of action. Philos Trans R Soc Lond B Biol Sci 355: 1771‐1788, 2000.
 52.Fuentes CT, Bastian AJ. Where is your arm? Variations in proprioception across space and tasks. J Neurophysiol 103: 164‐171, 2010.
 53.Gandevia SC. Illusory movements produced by electrical stimulation of low‐threshold muscle afferents from the hand. Brain 108: 965‐981, 1985.
 54.Gandevia SC. Kinesthesia: Roles for afferent signals and motor commands. In: Rowell LB, Shepherd JT, editors. Handbook of Physiology Section 12 Exercise: Regulation and Integration of Multiple Systems. Oxford: Oxford University Press, 1996, pp. 128‐172.
 55.Gandevia SC, Phegan CM. Perceptual distortions of the human body image produced by local anaesthesia, pain and cutaneous stimulation. J Physiol 514: 609‐616, 1999.
 56.Gandevia SC, Smith JL, Crawford M, Proske U, Taylor JL. Motor commands contribute to human position sense. J Physiol 571: 703‐710, 2006.
 57.Gelfan S, Carter S. Muscle sense in man. Exp Neurol 18: 469‐473, 1967.
 58.Georgopoulos AP, Schwartz AB, Kettner RE. Neuronal population coding of movement direction. Science 233: 1416‐1419, 1986.
 59.Ghez C, Gordon J, Ghilardi MF. Impairments of reaching movements in patients without proprioception. II. Effects of visual information on accuracy. J Neurophysiol 73: 361‐372, 1995.
 60.Gilhodes JC, Roll JP, Tardy‐Gervet MF. Perceptual and motor effects of agonist‐antagonist muscle vibration in man. Exp Brain Res 61: 395‐402, 1986.
 61.Giummarra MJ, Gibson SJ, Georgiou‐Karistianis N, Bradshaw JL. Central mechanisms in phantom limb perception: The past, present and future. Brain Res Rev 54: 219‐232, 2007.
 62.Goodmurphy CW, Ovalle WK. Morphological study of two human facial muscles: Orbicularis oculi and corrugator supercilii. Clin Anat 12: 1‐11, 1999.
 63.Goodwin GM, McCloskey DI, Matthews PBC. The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. Brain 95: 705‐748, 1972.
 64.Gooey K, Bradfield O, Talbot J, Morgan DL, Proske U. Effects of body orientation, load and vibration on sensing position and movement at the human elbow joint. Exp Brain Res 133: 340‐348, 2000.
 65.Gregory JE, Morgan DL, Proske U. Aftereffects in the responses of cat muscle spindles. J Neurophysiol 56: 451‐461, 1986.
 66.Gregory JE, Morgan DL, Proske U. Aftereffects in the responses of cat muscle spindles and errors of limb position sense in man. J Neurophysiol 59: 1220‐1230, 1988.
 67.Gregory JE, Morgan DL, Proske U. Responses of muscle spindles depend on their history of activation and movement. Prog Brain Res 74: 85‐90, 1988.
 68.Gregory JE, Morgan DL, Proske U. Two kinds of resting discharge in cat muscle spindles. J Neurophysiol 66: 602‐612, 1991.
 69.Guardia D, Conversy L, Jardri R, Lafargue G, Thomas P, Dodin V, Cottencin O, Luyat M. Imagining one's own and someone else's body actions: dissociation in anorexia nervosa. PLoS One 7: e43241, 2012.
 70.Guerraz M, Provost S, Narison R, Brugnon A, Virolle S, Bresciani JP. Integration of visual and proprioceptive afferents in kinesthesia. Neuroscience 223: 258‐268, 2012.
 71.Hagbarth K‐E, Eklund G. Motor effects of vibratory stimuli in man. In: Granit R, editor. Muscular Afferents and Motor Control. London: Wiley, 1966, pp. 177‐186.
 72.Hagura N, Takei T, Hirose S, Aramaki Y, Matsumura M, Sadato N, Naito E. Activity in the posterior parietal cortex mediates visual dominance over kinesthesia. J Neurosci 27: 7047‐7053, 2007.
 73.Hakuta N, Izumizaki M, Kigawa K, Murai N, Atsumi T, Homma I. Proprioceptive illusions created by vibration of one arm are altered by vibrating the other arm. Exp Brain Res 232: 2197‐2206, 2014.
 74.Hall LA, McCloskey DI. Detections of movements imposed on finger, elbow and shoulder joints. J Physiol 335: 519‐533, 1983.
 75.Halsband U, Schmitt J, Weyers M, Binkofski F, Grutzner G, Freund HJ. Recognition and imitation of pantomimed motor acts after unilateral parietal and premotor lesions: A perspective on apraxia. Neuropsychologia 39: 200‐216, 2001.
 76.Happak W, Burggasser G, Liu J, Gruber H, Freilinger G. Anatomy and histology of the mimic muscles and the supplying facial nerve. Eur Arch Otorhinolaryngol S85‐S86, 1994.
 77.Harrison PJ. After‐effects following responses of a muscle stretch receptor of the shore crab, Carcinus maenas. Neurosci Lett 88: 211‐215, 1988.
 78.Head H, Holmes G. Sensory disturbances from cerebral lesions. Brain 34: 102‐254, 1911.
 79.Helmholtz Hv. Helmholtz's Treatise on Physiological Optics, vol. 3. Menasha, Wisconsin: Optical Society of America, 1867.
 80.Herbert RD, Héroux ME, Diong J, Bilston LE, Gandevia SC, Lichtwark GA. Changes in the length and three‐dimensional orientation of muscle fascicles and aponeuroses with passive length changes in human gastrocnemius muscles. J Physiol 593: 441‐455, 2015.
 81.Héroux ME, Bayle N, Butler AA, Gandevia SC. Time, touch and temperature affect perceived finger position and ownership in the grasp illusion. J Physiol 596: 267‐280, 2018.
 82.Héroux ME, Walsh LD, Butler AA, Gandevia SC. Is this my finger? Proprioceptive illusions of body ownership and representation. J Physiol 591: 5661‐5670, 2013.
 83.Hill DK. Tension due to interaction between the sliding filaments in resting striated muscle. The effect of stimulation. J Physiol 199: 637‐684, 1968.
 84.Holmes NP, Crozier G, Spence C. When mirrors lie: “Visual capture” of arm position impairs reaching performance. Cogn Affect Behav Neurosci 4: 193‐200, 2004.
 85.Holst Hv. Relations between the central nervous system and the peripheral organs. Brit J Anim Behav 2: 89‐94, 1954.
 86.Hospod V, Aimonetti JM, Roll JP, Ribot‐Ciscar E. Changes in human muscle spindle sensitivity during a proprioceptive attention task. J Neurosci 27: 5172‐5178, 2007.
 87.Hutton RS, Smith JL, Eldred E. Postcontraction sensory discharge from muscle and its source. J Neurophysiol 36: 1090‐1103, 1973.
 88.Inui N, Masumoto J, Beppu T, Shiokawa Y, Akitsu H. Loss of large‐diameter nerve sensory input changes perceived posture. Exp Brain Res 221: 369‐375, 2012.
 89.Inui N, Walsh LD, Taylor JL, Gandevia SC. Dynamic changes in the perceived posture of the hand during ischaemic anaesthesia of the arm. J Physiol 589: 5775‐5784, 2011.
 90.Izumizaki M, Tsuge M, Akai L, Proske U, Homma I. The illusion of changed position and movement from vibrating one arm is altered by vision or movement of the other arm. J Physiol 588: 2789‐2800, 2010.
 91.Jones EG. The development of the ‘muscular sense’ concept during the nineteenth century and the work of H. Charlton Bastian. J Hist Med Allied Sci 27: 298‐311, 1972.
 92.Jones KE, Wessberg J, Vallbo A. Proprioceptive feedback is reduced during adaptation to a visuomotor transformation: Preliminary findings. Neuroreport 12: 4029‐4033, 2001.
 93.Kalckert A, Ehrsson HH. Moving a rubber hand that feels like your own: A dissociation of ownership and agency. Front Hum Neurosci 6: 40, 2012.
 94.Kammers MP, Longo MR, Tsakiris M, Dijkerman HC, Haggard P. Specificity and coherence of body representations. Perception 38: 1804‐1820, 2009.
 95.Kammers MP, van der Ham IJ, Dijkerman HC. Dissociating body representations in healthy individuals: Differential effects of a kinaesthetic illusion on perception and action. Neuropsychologia 44: 2430‐2436, 2006.
 96.Kerkhoff G. Spatial hemineglect in humans. Prog Neurobiol 63: 1‐27, 2001.
 97.Kigawa K, Izumizaki M, Tsukada S, Hakuta N. Proprioceptive interaction between the two arms in a single‐arm pointing task. PLoS One 10: e0137031, 2015.
 98.Lackner JR. Some proprioceptive influences on the perceptual representation of body shape and orientation. Brain 111: 281‐297, 1988.
 99.Lackner JR, Levine MS. Changes in apparent body orientation and sensory localization induced by vibration of postural muscles: Vibratory myesthetic illusions. Aviat Space Environ Med 50: 346‐354, 1979.
 100.Lackner JR, Taublieb AB. Influence of vision on vibration‐induced illusions of limb movement. Exp Neurol 85: 97‐106, 1984.
 101.Landgren S, Silfvenius H. Projection to cerebral cortex of group I muscle afferents from the cat's hind limb. J Physiol 200: 353‐372, 1969.
 102.Longo MR, Cardozo S, Haggard P. Visual enhancement of touch and the bodily self. Conscious Cogn 17: 1181‐1191, 2008.
 103.Longo MR, Haggard P. An implicit body representation underlying human position sense. Proc Natl Acad Sci U S A 107: 11727‐11732, 2010.
 104.Longo MR, Kammers MP, Gomi H, Tsakiris M, Haggard P. Contraction of body representation induced by proprioceptive conflict. Curr Biol 19: R727‐R728, 2009.
 105.Longo MR, Schuur F, Kammers MP, Tsakiris M, Haggard P. What is embodiment? A psychometric approach. Cognition 107: 978‐998, 2008.
 106.Macefield G, Gandevia SC, Burke D. Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. J Physiol 429: 113‐129, 1990.
 107.Matthews PBC. Proprioceptors and their contribution to somatosensory mapping: Complex messages require complex processing. Can J Physiol Pharmacol 66: 430‐438, 1988.
 108.McCloskey DI. Differences between the senses of movement and position shown by the effects of loading and vibration of muscles in man. Brain Res 61: 119‐131, 1973.
 109.McCloskey DI. Position sense after surgical disconnexion of the cerebral hemispheres in man. Brain 96: 269‐276, 1973.
 110.McCloskey DI, Cross MJ, Honner R, Potter EK. Sensory effects of pulling or vibrating exposed tendons in man. Brain 106(Pt 1): 21‐37, 1983.
 111.McIntyre AK. Central actions of impulses in muscle afferent fibres. In: Hunt CC, editor. Handbook of Sensory Physiology: Muscle Receptors. Berlin: Springer, 1974, pp. 235‐288.
 112.McIntyre AK, Holman ME, Veale JL. Cortical responses to impulses from single Pacinian corpuscles in the cat's hind limb. Exp Brain Res 4: 243‐255, 1967.
 113.Medina J, Duckett C. Domain‐general biases in spatial localization: evidence against a distorted body model hypothesis. J Exp Psychol Hum Percept Perform 43: 1430‐1443, 2017.
 114.Melzack R. Phantom limbs and the concept of a neuromatrix. Trends Neurosci 13: 88‐92, 1990.
 115.Melzack R, Israel R, Lacroix R, Schultz G. Phantom limbs in people with congenital limb deficiency or amputation in early childhood. Brain 120: 1603‐1620, 1997.
 116.Merton PA. Human position sense and sense of effort. Symp Soc Exp Biol 18: 387‐400, 1964.
 117.Metral M, Chancel M, Brun C, Luyat M, Kavounoudias A, Guerraz M. Kinaesthetic mirror illusion and spatial congruence. Exp Brain Res 233: 1463‐1470, 2015.
 118.Moberg E. The role of cutaneous afferents in position sense, kinaesthesia, and motor function of the hand. Brain 106(Pt 1): 1‐19, 1983.
 119.Morgan DL, Prochazka A, Proske U. The after‐effects of stretch and fusimotor stimulation on the responses of primary endings of cat muscle spindles. J Physiol 356: 465‐477, 1984.
 120.Morgan DL, Proske U, Gregory JE. Responses of primary endings of cat muscle spindles to locally applied vibration. Exp Brain Res 87: 530‐536, 1991.
 121.Naito E, Ehrsson HH. Somatic sensation of hand‐object interactive movement is associated with activity in the left inferior parietal cortex. J Neurosci 26: 3783‐3790, 2006.
 122.Naito E, Morita T, Amemiya K. Body representations in the human brain revealed by kinesthetic illusions and their essential contributions to motor control and corporeal awareness. Neurosci Res 104: 16‐30, 2016.
 123.Naito E, Roland PE, Grefkes C, Choi HJ, Eickhoff S, Geyer S, Zilles K, Ehrsson HH. Dominance of the right hemisphere and role of area 2 in human kinesthesia. J Neurophysiol 93: 1020‐1034, 2005.
 124.Nierula B, Martini M, Matamala‐Gomez M, Slater M, Sanchez‐Vives MV. Seeing an embodied virtual hand is analgesic contingent on colocation. J Pain 18: 645‐655, 2017.
 125.Ortiz‐Catalan M, Guethmundsdottir RA, Kristoffersen MB, Zepeda‐Echavarria A, Caine‐Winterberger K, Kulbacka‐Ortiz K, Widehammar C, Eriksson K, Stockselius A, Ragno C, Pihlar Z, Burger H, Hermansson L. Phantom motor execution facilitated by machine learning and augmented reality as treatment for phantom limb pain: A single group, clinical trial in patients with chronic intractable phantom limb pain. Lancet 388: 2885‐2894, 2016.
 126.Oscarsson O, Rosen I. Projection to cerebral cortex of large muscle‐spindle afferents in forelimb nerves of the cat. J Physiol 169: 924‐945, 1963.
 127.Paillard J, Brouchon M. Active and passive movements in the calibration of position sense. In: Freedman S, editor. The Neuropsychology of Spatially Oriented Behaviour. Homewood, IL: Dorsey Press, 1968, pp. 37‐55.
 128.Paradiso GO, Cunic DI, Gunraj CA, Chen R. Representation of facial muscles in human motor cortex. J Physiol 567: 323‐336, 2005.
 129.Penfield W, Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60: 389‐443, 1937.
 130.Prochazka A, Ellaway P. Sensory systems in the control of movement. Compr Physiol 2: 2615‐2627, 2012.
 131.Prochazka A, Gorassini M. Ensemble firing of muscle afferents recorded during normal locomotion in cats. J Physiol 507(Pt 1): 293‐304, 1998.
 132.Proske U. The distribution and abundance of muscle spindles. Brain Res Bull 75: 502‐503, 2008.
 133.Proske U. The role of muscle proprioceptors in human limb position sense: A hypothesis. J Anat 227: 178‐183, 2015.
 134.Proske U, Gandevia SC. The kinaesthetic senses. J Physiol 587: 4139‐4146, 2009.
 135.Proske U, Gandevia SC. The proprioceptive senses: Their roles in signaling body shape, body position and movement, and muscle force. Physiol Rev 92: 1651‐1697, 2012.
 136.Proske U, Gregory JE, Morgan DL. Where in the muscle spindle is the resting discharge generated? Exp Physiol 76: 777‐785, 1991.
 137.Proske U, Morgan DL, Gregory JE. Thixotropy in skeletal muscle and in muscle spindles: A review. Prog Neurobiol 41: 705‐721, 1993.
 138.Proske U, Tsay A, Allen T. Muscle thixotropy as a tool in the study of proprioception. Exp Brain Res 232: 3397‐3412, 2014.
 139.Rabin E, Gordon AM. Influence of fingertip contact on illusory arm movements. J Appl Physiol 96: 1555‐1560, 2004.
 140.Ramachandran VS, Altschuler EL. The use of visual feedback, in particular mirror visual feedback, in restoring brain function. Brain 132: 1693‐1710, 2009.
 141.Ribot‐Ciscar E, Hospod V, Roll JP, Aimonetti JM. Fusimotor drive may adjust muscle spindle feedback to task requirements in humans. J Neurophysiol 101: 633‐640, 2009.
 142.Roll J, Gilhodes J, Roll R, Harlay F. Are proprioceptive sensory inputs combined into a “gestalt”? Vibration‐induced virtual hand drawing or visual target motion. In: Inui T, McClelland JL, editors. Attention and Performance. London: MIT Press, 1996, pp. 291‐314.
 143.Roll JP, Vedel JP. Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography. Exp Brain Res 47: 177‐190, 1982.
 144.Roll JP, Vedel JP, Ribot E. Alteration of proprioceptive messages induced by tendon vibration in man: A microneurographic study. Exp Brain Res 76: 213‐222, 1989.
 145.Romaiguere P, Anton JL, Roth M, Casini L, Roll JP. Motor and parietal cortical areas both underlie kinaesthesia. Brain Res Cogn Brain Res 16: 74‐82, 2003.
 146.Seizova‐Cajic T, Azzi R. Conflict with vision diminishes proprioceptive adaptation to muscle vibration. Exp Brain Res 211: 169‐175, 2011.
 147.Seizova‐Cajic T, Taylor JL. Somatosensory space abridged: Rapid change in tactile localization using a motion stimulus. PLoS One 9: e90892, 2014.
 148.Sherrington C. On the proprio‐ceptive system, especially in its reflex aspects. Brain 29: 467‐482, 1906.
 149.Shibuya S, Unenaka S, Ohki Y. Body ownership and agency: Task‐dependent effects of the virtual hand illusion on proprioceptive drift. Exp Brain Res 235: 121‐134, 2017.
 150.Skoglund S. Joint receptors and kinaesthesis. In: Iggo A, editor. Handbook of Sensory Physiology. Berlin: Springer, 1973, pp. 111‐136.
 151.Smith JL, Crawford M, Proske U, Taylor JL, Gandevia SC. Signals of motor command bias joint position sense in the presence of feedback from proprioceptors. J Appl Physiol 106: 950‐958, 2009.
 152.Stein RB, Weber DJ, Aoyagi Y, Prochazka A, Wagenaar JB, Shoham S, Normann RA. Coding of position by simultaneously recorded sensory neurones in the cat dorsal root ganglion. J Physiol 560: 883‐896, 2004.
 153.Taylor JL, McCloskey DI. Detection of slow movements imposed at the elbow during active flexion in man. J Physiol 457: 503‐513, 1992.
 154.Taylor JL, McCloskey DI. Illusions of head and visual target displacement induced by vibration of neck muscles. Brain 114(Pt 2): 755‐759, 1991.
 155.Taylor MW, Taylor JL, Seizova‐Cajic T. Muscle vibration‐induced illusions: Review of contributing factors, taxonomy of illusions and user's guide. Multisensory Research 30: 25‐63, 2017.
 156.Thieme H, Morkisch N, Rietz C, Dohle C, Borgetto B. The efficacy of movement representation techniques for treatment of limb pain–‐a systematic review and meta‐analysis. J Pain 17: 167‐180, 2016.
 157.Thyrion C, Roll JP. Predicting any arm movement feedback to induce three‐dimensional illusory movements in humans. J Neurophysiol 104: 949‐959, 2010.
 158.Timms J, Carus C. Mirror therapy for the alleviation of phantom limb pain following amputation: A literature review. Int J Ther Rehabil 22: 135‐145, 2017.
 159.Tsakiris M, Haggard P. The rubber hand illusion revisited: Visuotactile integration and self‐attribution. J Exp Psychol Hum Percept Perform 31: 80‐91, 2005.
 160.Tsay A, Allen TJ, Proske U. Position sense at the human elbow joint measured by arm matching or pointing. Exp Brain Res 234: 2787‐2798, 2016.
 161.Tsay A, Allen TJ, Proske U. Position sense at the human forearm after conditioning elbow muscles with isometric contractions. Exp Brain Res 233: 2635‐2643, 2015.
 162.Tsay A, Savage G, Allen TJ, Proske U. Limb position sense, proprioceptive drift and muscle thixotropy at the human elbow joint. J Physiol 592: 2679‐2694, 2014.
 163.Tsay AJ, Giummarra MJ, Allen TJ, Proske U. The sensory origins of human position sense. J Physiol 594: 1037‐1049, 2016.
 164.Tsuge M, Izumizaki M, Kigawa K, Atsumi T, Homma I. Interaction between vibration‐evoked proprioceptive illusions and mirror‐evoked visual illusions in an arm‐matching task. Exp Brain Res 223: 541‐551, 2012.
 165.Vallar G, Ronchi R. Somatoparaphrenia: A body delusion. A review of the neuropsychological literature. Exp Brain Res 192: 533‐551, 2009.
 166.Vallbo AB. Human muscle spindle discharge during isometric voluntary contractions. Amplitude relations between spindle frequency and torque. Acta Physiol Scand 90: 319‐336, 1974.
 167.Velay JL, Roll R, Paillard J. Elbow position sense in man: contrasting results in matching and pointing. Hum Movement Sci 8: 177‐193, 1989.
 168.Walsh LD, Gandevia SC, Taylor JL. Illusory movements of a phantom hand grade with the duration and magnitude of motor commands. J Physiol 588: 1269‐1280, 2010.
 169.Walsh LD, Moseley GL, Taylor JL, Gandevia SC. Proprioceptive signals contribute to the sense of body ownership. J Physiol 589: 3009‐3021, 2011.
 170.Walsh LD, Proske U, Allen TJ, Gandevia SC. The contribution of motor commands to position sense differs between elbow and wrist. J Physiol 591: 6103‐6114, 2013.
 171.Wann JP, Ibrahim SF. Does limb proprioception drift? Exp Brain Res 91: 162‐166, 1992.
 172.Weiss PH, Dohle C, Binkofski F, Schnitzler A, Freund HJ, Hefter H. Motor impairment in patients with parietal lesions: Disturbances of meaningless arm movement sequences. Neuropsychologia 39: 397‐405, 2001.
 173.White O, Proske U. Illusions of forearm displacement during vibration of elbow muscles in humans. Exp Brain Res 192: 113‐120, 2009.
 174.Whitham EM, Fitzgibbon SP, Lewis TW, Pope KJ, Delosangeles D, Clark CR, Lillie P, Hardy A, Gandevia SC, Willoughby JO. Visual experiences during paralysis. Front Hum Neurosci 5: 160, 2011.
 175.Wilson LR, Gandevia SC, Burke D. Increased resting discharge of human spindle afferents following voluntary contractions. J Physiol 488: 833‐840, 1995.
 176.Winter JA, Allen TJ, Proske U. Muscle spindle signals combine with the sense of effort to indicate limb position. J Physiol 568: 1035‐1046, 2005.
 177.Wise AK, Gregory JE, Proske U. The effects of muscle conditioning on movement detection thresholds at the human forearm. Brain Res 735: 125‐130, 1996.
 178.Wise AK, Gregory JE, Proske U. The responses of muscle spindles to small, slow movements in passive muscle and during fusimotor activity. Brain Res 821: 87‐94, 1999.
 179.Zopf R, Contini E, Fowler C, Mondraty N, Williams MA. Body distortions in anorexia nervosa: Evidence for changed processing of multisensory bodily signals. Psychiatry Res 245: 473‐481, 2016.
 180.Zopf R, Savage G, Williams MA. Crossmodal congruency measures of lateral distance effects on the rubber hand illusion. Neuropsychologia 48: 713‐725, 2010.

 

Teaching Material

U. Proske, S. C. Gandevia. Kinesthetic Senses. Compr Physiol 8: 2018, 1157-1183.

Didactic Synopsis

Major Teaching Points:

  1. The two major kinesthetic senses are the sense of position of our body and the sense of movement.
  2. They can be measured in two ways:
    • Measure the size of an illusion of position and movement of our limbs by vibrating a muscle.
    • Measure changes in perceived position after contracting a muscle and stretching or shortening it.
  3. To measure the illusion, a blindfolded subject aligns one forearm with the other to indicate its location. Alternatively, the subject points to the position of one arm hidden from view.
  4. The kinesthetic senses combine with vision and touch to give us a sense of body ownership. This is linked to a sense of agency, “I am moving my arm.”
  5. Sensory and motor areas of the brain receive kinesthetic signals to tell us where our body parts are and where they are located in relation to our surroundings.

Didactic Legends

The figures—in a freely downloadable PowerPoint format—can be found on the Images tab along with the formal legends published in the article. The following legends to the same figures are written to be useful for teaching.

Figure 1 Muscle thixotropy. Teaching points: (A) The diagram shows a series of repeating units called sarcomeres. A string of sarcomeres is called a myofibril and each skeletal muscle fiber in our body is composed of bundles of myofibrils. The sarcomere is composed of thick longitudinal filaments of a protein, myosin (shown in blue), which attaches to the adjacent thin filaments of the protein actin (shown in black) by means of cross-bridges with grape-like heads. During a muscle contraction, all of these heads attach to the actin and rotate, in the process pulling the two halves of a sarcomere towards one another and generating force. At the end of a contraction, as the muscle relaxes, the myosin heads detach from the actin. Subsequently a few, randomly scattered, heads reattach (shown in red), but they do not go through the usual rotation process to generate force. They remain attached for as long as the muscle is left undisturbed. They give the muscle a resting stiffness whose value depends on whether the muscle has been previously moved or not. Such history-dependent behavior is called thixotropy. (B) These are records of the length (blue) and tension (red) changes in a passive muscle showing thixotropic behavior during stretch and shortening movements. During muscle lengthening (upward moving blue ramp on the left), passive tension rises steeply, as the attached cross-bridges (red in A) are stressed by the stretch. A point is reached at peak tension where stress is sufficient to lead to detachment of the cross-bridges from actin and tension begins to fall. When a shortening is applied to the muscle (downward blue ramp on the right), the presence of attached cross-bridges (red in A), exert a splinting effect, preventing the muscle from fully shortening and it falls slack. This pushing effect by the attached cross-bridges leads to the precipitous fall in tension.

Figure 2 Teaching points: (A) Flexion conditioning. This is a method of placing the muscles of the human forearm in a defined state with respect to the thixotropic behavior of muscle stretch receptors, the muscle spindles, which are known to signal muscle length, that is, limb position. A blindfolded subject sits at a table, which supports both forearms. The arms have been taped to paddles hinged at a point aligned with the subject's elbow joints. Potentiometers at the hinges provide signals of elbow angles (see Figure 5). The subject is asked to relax while the experimenter moves one forearm into a vertical position (conditioning angle). The subject is then asked to contract their elbow flexor muscles by trying to pull the arm towards their body, while it is held in position by the experimenter. The contraction leads to sensitization of elbow flexor muscle spindles, as a result of their thixotropic property. After the arm has relaxed, when the experimenter extends it to the test angle (actual), this stretches the muscle spindles and they generate a strong position signal. This shows up when the subject is asked to match position of the arm with their other arm, which they place into a more extended position (perceived angle) than the actual position of the arm. (B) Extension conditioning. This is a similar procedure to that in A, but the starting point is the relaxed arm lying on the table. The subject is asked to push down on the table, in the process contracting elbow extensor muscles and sensitizing their muscle spindles (conditioning angle). The experimenter then flexes the arm, moving it to the test angle (actual) and the subject is asked to indicate location of the arm by matching its position with their other arm. As a result of the sensitization of muscle spindles, the subject thinks their extensors are more stretched, the elbow more flexed than is really the case. They, therefore, adopt a too flexed matching position with the other arm (perceived angle).

Figure 3 Distribution of position errors at the forearm from different forms of thixotropic conditioning. Teaching points: The figure shows the variety of position errors that can be generated at the human forearm as a result of thixotropic conditioning of arm muscles. All measurements of errors are by blindfolded subjects matching positions of their forearms, using the apparatus described in Figure 5A. The pair of position errors shown on the left has been measured for groups of subjects whose arms had both been flexion conditioned (blue symbol) or extension conditioned (red symbol), as shown in Figure 2. After flexion conditioning, spindles in flexor muscles of both arms have been sensitized. This leads to small matching errors in the direction of elbow flexion (blue symbol). Errors are not zero because of movement related spindle activity in the indicator arm moving into the matching position. It leads the subject to declare a match too soon, with the indicator still too flexed and before the arms are truly aligned. The same reasoning is applied to the generation of small errors into extension after extension conditioning of both arms (red symbol). The middle pair of values in the figure shows the distribution of errors when the two arms are conditioned differently from one another. One arm has both its extensor and flexor muscles co-conditioned, that is, the arm is brought to the test angle and its flexors and then extensors are contracted while the arm is held fixed in position (see Figure 4). The perceived position of the arm is indicated with the other arm, which has been flexion, conditioned or extension conditioned (Figure 2). For the co-conditioned arm, because spindle signals in both antagonist muscles are similarly sensitized, this leads to a low difference signal, that is, a low position signal. The other arm used to indicate this position has been only flexion or extension conditioned and so it has a high flexor or extensor signal. When the subject is trying to match arm positions with one arm that has a high flexor signal and the other a low signal, the subject keeps their flexor conditioned arm as flexed as possible, trying to generate a low matching signal. As a result, large errors into flexion result (blue symbol). Similarly, large errors in the direction of extension (red symbol) are generated when the indicator arm is extension conditioned. The right-hand pair of data points demonstrate that muscle conditioning can be arranged to achieve position errors that lie close to zero. Here for both error values the reference arm has been brought to the test angle and its muscles co-conditioned (see Figure 4), leading to a low position signal in that arm. To match this, it is necessary to lower the position signal in the other arm as well. That is done by introducing slack in its muscle spindles. For a flexion-conditioned arm (Figure 2), after the conditioning contraction and sensitization of flexor spindles, the arm is fully extended before being returned to the matching position. Flexion of the arm after the extension means that flexor spindles are shortened and because of their thixotropic property they are unable to shorten themselves and they fall slack (Figure 1). A slack spindle has no tension on its sensory ending and so its prevailing activity falls to low levels. Now, during the match both arms have low position signals and the error (blue symbol) is small. A similar outcome can be achieved when the indicator arm is extension conditioned. Here, after the conditioning contraction in the extended position (Figure 2), the arm is brought into full flexion before being returned to the matching position. The extension movement from flexion to the matching position introduces slack in extensor spindles and their low level of activity matches that in the co-conditioned arm (red symbol).

Figure 4 Test angle co-conditioning. Teaching points: It is known that it is not the absolute level of discharge coming from muscle spindles of one muscle of the forearm that determines the forearm position signal, but the difference in signal between the two antagonists, the flexors, and extensors. Co-conditioning is a method of conditioning of the two antagonists so that both are left in a near identical state, leading to a low nett position signal coming from the arm. The blindfolded subject has their forearm placed at the test angle by the experimenter and they are asked to contract their elbow flexors by trying to pull the forearm toward the body and then their extensors by trying to push the arm away from the body while it is being held in position by the experimenter. Once the two contractions have been completed and the subject has relaxed their arm, its position is indicated with the other arm. The perceived position (perceived angle) lies close to the true position (actual).

Figure 5 Measuring position sense in matching and pointing tasks. Teaching points: (A) Matching task. Position sense at the forearm can be measured by the experimenter placing a blindfolded subject's arm (reference) at a test angle and the subject is asked to match its position by placement of their other (indicator) arm. This form of position matching is really a sensation-matching task, in which the subject moves their indicator arm until the sensations arising in it match those coming from the reference. Muscle spindles in muscles acting at the elbow are believed to provide the position signal. Because spindles exhibit thixotropic behavior, it is necessary to put both arms into a thixotropically defined state before such measurements are made. (B) Pointing task. Intuitively, we do not typically determine the position of one of our arms in space by mimicking its position with the other arm. Rather, we point to where we think the arm is located. This is a very different task to one involving sensation matching. In pointing no comparison of sensory signals between the arms is possible and the evidence suggests that in this form of position location muscle spindles are not involved. In the experimental arrangement, one arm (reference) is hidden from view behind a screen while the subject moves a paddle (pointer) to align its position with that of the reference.

Figure 6 Position errors in matching and pointing tasks. Teaching points: (A) Matching task. A plot of the distribution of errors when the position of one arm is indicated by placement of the blindfolded subject's other arm into a matching position (Figure 5A). To make sure that the muscle spindles believed to be responsible for this sense are in a comparable thixotropic state in elbow muscles of both arms, both are first flexion or extension conditioned (Figure 2). The prediction for flexion conditioning is small errors into flexion, for extension conditioning small errors into extension (Figure 3). The predicted errors (blue symbols) lie close to the actually measured errors (red symbols). In other words, the distribution of position errors in a matching task is consistent with predictions based on the properties of the position sensors, the muscle spindles. (B) Pointing task. Here position errors are measured in a pointing task where the subject aligns a pointer with the perceived position of their other arm, which remains hidden from view (Figure 5B). Assuming that in position sense measured in this way muscle spindles in elbow muscles of the hidden arm provide the position signal, after flexion conditioning (Figure 2A) significant errors into extension are expected. This distribution is different from that in A mentioned earlier because only one arm is involved. The observed errors (red symbol, left) are consistent with predictions (blue symbol, left). That, however, is not the case for extension conditioning of the arm (Figure 2B). Here the prediction is for large errors into flexion (blue symbol, right) and what is observed is large errors into extension (red symbol, right), the opposite direction to expectations. The conclusion from this experiment is that the distribution of position errors in a one-arm-pointing task no longer conforms to predictions based on the known behavior of muscle spindles. The broader conclusion is that muscle spindle signals do not contribute to limb position sense measured by pointing.

Figure 7 Teaching points: The diagram shows the way in which the experiments are conducted for the study of the perceived vertical distance between the index fingers in the vertical plane, the extent to which the subjects believe that they are holding their right index finger with their left hand (a measure of body ownership). The right forearm of the subject is positioned on the lower table so that the end of the index finger is held comfortably in a padded pipe, which can only rotate around the proximal interphalangeal joint. In one study, in which the left hand is not involved, the subject cannot see an artificial index finger which is part of the upper table and which can be rotated by the experimenter. Depending on whether the coupling between the upper and lower tables is fixed or not, the movement can be directly coupled so that the right index finger moves together with the artificial finger (congruent movement) or it can be uncoupled so that the motion of the two fingers occurs together and is incongruent. The vertical distance between the right index finger and the artificial finger is 12 cm. In another study, vision was excluded (see screen) and the experimenter lightly held the subject's left index finger and thumb against an object (actually the artificial finger). Congruent or incongruent movement was delivered to the right index finger and the artificial finger being held by the left index finger and thumb.

Figure 8 Teaching points: (A) The diagram shows subjective ratings on a 7-point scale of the subjects’ belief that they were holding their right index finger with their left hand under two conditions. All measures were made after the right index finger, and left index finger and thumb (which were touching the artificial finger) were locally anaesthetized. This meant that no information from the fingers could influence judgments. Proximal muscles in the hand and forearm were not affected by this procedure and information from them could be used by the brain. When movements of the index fingers on the two hands (and the artificial finger) were moved together in a congruent way, the subjects agreed that they were holding their right index finger with their left hand. They disagreed with this statement when the movements were made in an incongruent way. (B) This diagram shows the perceived spacing in the vertical plane between the left and right index fingers in the same study as in Panel A. Again, the right index finger and the left index finger and thumb were anaesthetized. When the movements of the index fingers on the two hands (and the artificial finger) were congruent, the subjects perceived that the vertical spacing between them was only approximately 2 cm. However, this perceived vertical distance was greater when the movements were incongruent (approximately 4 cm). Again, the true perceived distance between the index fingers was 12 cm. Thus, simply grasping the finger-like object without vision being available is sufficient to shrink the perceived distance between the left and right index fingers.

 


Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Kinesthetic Senses
 

How to Cite

Uwe Proske, Simon C. Gandevia. Kinesthetic Senses. Compr Physiol 2018, 8: 1157-1183. doi: 10.1002/cphy.c170036