Skip to main content
Log in

Effect of slow, small movement on the vibration-evoked kinesthetic illusion

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The study reported in this paper investigated how vibration-evoked illusions of joint rotation are influenced by slow (0.3°/s), small (2–4°) passive rotation of the joint. Normal human adults (n=15) matched the perceived position of the left (“reference”) arm with the right (“matching”) arm while vibration (50 pps, 0.5 mm) was applied for 30 s to the relaxed triceps brachii of the reference arm. Both arms were constrained to rotate horizontally at the elbow. Three experimental conditions were investigated: (1) vibration of the stationary reference arm, (2) slow, small passive extension or flexion of the reference arm during vibration, and (3) slow, small passive extension or flexion of the reference arm without vibration. Triceps brachii vibration at 50 pps induced an illusion of elbow flexion. The movement illusion began after several seconds, relatively fast to begin with and gradually slowing down to a stop. On average, triceps vibration produced illusory motion at an average latency of 6.3 s, amplitude of 9.7°, velocity of 0.6°/s, and duration of 16.4 s. During vibration, slow, small (≈0.3°/s, 1.3°) passive rotations of the joint dramatically enhanced, stopped, or reversed the direction of illusory movement, depending on the direction of the passive joint rotation. However, the subjects’ perceptions of these passive elbow rotations were exaggerated: 2–3 times the size of the actual movement. In the absence of vibration, the subjects accurately reproduced these passive joint rotations. We discuss whether the exaggerated perception of slow, small movement during vibration is better explained by contributions of non muscle spindle Ia afferents or by changes in the mechanical transmission of vibration to the receptor.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abrahams VC (1986) Group II and IV receptors of skeletal muscle. Can J Physiol Pharmacol 64:509–514

    PubMed  CAS  Google Scholar 

  • van Beekum WT (1980) The participation of muscle spindles in human position sense studied by mechanical vibration of muscles. Thesis

  • Bianconi R, Van der Meulen JP (1963) The response to vibration of the end-organs of mammalian muscle spindles. J Neurophysiol 26:177–190

    PubMed  CAS  Google Scholar 

  • Brown MC, Engberg I, Mattews PBC (1967) The relative sensitivity to vibration of muscle receptors of the cat. J Physiol 192:773–800

    PubMed  CAS  Google Scholar 

  • Brumagne S, Gurfinkel VS, Flores-Vieira C, Cordo PC, Roberts W (2000) Vibration-induced kinesthetic illusions: a conflict between natural and artificial afferent inflow. Soc Neurosci Abstr, Vol 26, Pt I, p. 1230

  • Burgess PR, Clark FJ (1969) Characteristics of knee joint receptors in the cat. J Physiol 203:317–335

    PubMed  CAS  Google Scholar 

  • Burke D, Eklund G (1977) Muscle spindle activity in man during standing. Acta physiol scand 100:187–199

    PubMed  CAS  Google Scholar 

  • Burke D, Hagbarth K-E, Löfstedt L, Wallin BG (1976) The responses of human muscle spindle endings to vibration of non-contracting muscles. J Physiol 261:673–693

    PubMed  CAS  Google Scholar 

  • Calvin-Figuière S, Romaiguère P, Gilhodes JC, Roll JP (1999) Antagonist motor responses correlate with kinesthetic illusions induced by tendon vibration. Exp Brain Res 124:342–350

    Article  PubMed  Google Scholar 

  • Colebatch JG, Sayer RJ, Porter R, White OB (1990) Responses of monkey precentral neurons to passive movements and phasic muscle stretch: relevance to man. Electroenceph clin Neurophysiol 75:44–55

    Article  PubMed  CAS  Google Scholar 

  • Collins DF, Prochazka A (1996) Movement illusions evoked by ensemble cutaneous input from the dorsum of the hand. J Physiol 496:857–871

    PubMed  CAS  Google Scholar 

  • Collins DF, Refshauge KM, Gandevia SC (2000) Sensory integration in the perception of movements at the human metacarpophalangeal joint. J Physiol 529:505–515

    Article  PubMed  CAS  Google Scholar 

  • Cordo PJ, Gandevia SC, Hales JP, Burke D, Laird G (1993) Force and displacement-controlled tendon vibration in humans. EEG Clin Neurophysiol 89:45–53

    CAS  Google Scholar 

  • Cordo P, Gurfinkel V, Bevan L, Kerr GK (1995) Proprioceptive consequences of tendon vibration during movement. J Neurophysiol 74:1675–1688

    PubMed  CAS  Google Scholar 

  • Craske B (1977) Perception of impossible limb position induced by tendon vibration. Science 196:71–73

    Article  PubMed  CAS  Google Scholar 

  • Crowe A, Matthews PBC (1964) Further studies of static and dynamic fusimotor fibres. J Physiol 174:132–151

    PubMed  CAS  Google Scholar 

  • Driver J, Spence C (1998) Attention and crossmodal construction of space. Trends Cogn Sci 2:254–262

    Article  Google Scholar 

  • Echlin F, Fessard A (1938) Synchronized impulse discharges from receptors in the deep tissues in response to a vibrating stimulus. J Physiol 93:321–334

    Google Scholar 

  • Edin BB (1992) Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin. J Neurophysiol 67:1105–1113

    PubMed  CAS  Google Scholar 

  • Edin BB (2001) Cutaneous afferents provide information about knee joint movements in humans. J Physiol 531:289–297

    Article  PubMed  CAS  Google Scholar 

  • Edin BB, Abbs JH (1991) Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of the human hand. J Neurophysiol 65:657–670

    PubMed  CAS  Google Scholar 

  • Edin BB, Johansson N (1995) Skin strain patterns provide kinaesthetic information to the human central nervous system. J Physiol 487:243–251

    PubMed  CAS  Google Scholar 

  • Ferrell WR, Gandevia SC, McCloskey DI (1987) The role of joint receptors in human kinaesthesia when intramuscular receptors cannot contribute. J Physiol 386:63–71

    PubMed  CAS  Google Scholar 

  • Gandevia SC (1996) Kinesthesia: roles for afferent signals and motor commands. Handbook of physiology. In: Rowell LB, Shepherd JT (eds) Exercise: regulation and integration of multiple systems, Sect.12. Oxford, New York, pp 128–172

  • Gardener EP, Costanzo RM (1981) Properties of kinesthetic neurons in somatosensory cortex of awake monkeys. Brain Res 214:301–319

    Article  PubMed  Google Scholar 

  • Ge W, Khalsa PS (2003) Encoding of compressive stress during indentation by group III and IV muscle mechano-nociceptors in rat gracilis muscle. J Neurophysiol 89:785–792

    Article  PubMed  Google Scholar 

  • Goodwin GM, McCloskey DI, Matthews PB (1972) The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions and by the effects of paralysing joint afferents. Brain 95:705–748

    Article  PubMed  CAS  Google Scholar 

  • Granit R (1970) The basis of motor control. Academic, London

    Google Scholar 

  • Granit R, Henatsch HD (1956) Gamma control of dynamic properties of muscle spindles. J Neurophysiol 19:356–366

    PubMed  CAS  Google Scholar 

  • Grill SE, Hallett M (1995) Velocity sensitivity of human muscle spindle afferents and slowly adapting type II cutaneous mechanoreceptors. J Physiol 489:593–602

    PubMed  CAS  Google Scholar 

  • Hagbarth K-E, Eklund G (1966) Motor effects of vibratory muscle stimuli in man. In: Granit R (eds) Muscular afferents and motor control. Almqvist and Wiksell, Stockholm, pp 177–186

    Google Scholar 

  • Hall LA, McCloskey DI (1983) Detections of movements imposed on finger, elbow and shoulder joints. J Physiol 355:519–533

    Google Scholar 

  • Hoffman P (1922) Untersuchungen über die Eigenreflexe (Sehnenreflexe) menschlicher Muskeln. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Houk JC, Henneman E (1967) Responses of Golgi tendon organs to active contraction of the soleus muscle of the cat. J Neurophysiol 30:466–481

    PubMed  CAS  Google Scholar 

  • Inglis JT, Frank JS (1990) The effect of angonist/antagonist muscle vibration on human position sense. Exp Brain Res 81:573–580

    Article  PubMed  CAS  Google Scholar 

  • Johnson K (2004) Closing in on the neural mechanisms of finger joint angle sense. Focus on “Quantitative analysis of dynamic strain sensitivity in human skin mechanoreceptors. J Neurophysiol 92:3167–3168

    Article  PubMed  Google Scholar 

  • Kasai T, Kawanishi M, Yahai S (1994) Effects of upper limb muscle vibration on voluntary wrist flexion-extension movements. Percept Motor Skills 78:43–47

    PubMed  CAS  Google Scholar 

  • Lackner JR (1988) Some proprioceptive influences on the perceptual representation of body shape and orientation. Brain 111:281–297

    Article  PubMed  Google Scholar 

  • Lance JW, DeGail P, Neilson PD (1966) Tonic and phasic spinal cord mechanisms in man. J Neurol Neurosurg Psychiatry 29:535–544

    Google Scholar 

  • Macaluso E, Frith CD, Driver J (2000) Modulation of human visual cortex by crossmodal spatial attention. Science 289:1206–1208

    Article  PubMed  CAS  Google Scholar 

  • Matthews BHC (1933) Nerve endings in mammalian muscle. J Physiol 78:1–33

    PubMed  CAS  Google Scholar 

  • Matthews PBC (1982) Where does Sherrington’s “muscular sense” originate? Muscles, joints, corollary discharges?. Annu Rev Neurosci 5:189–218

    Article  PubMed  CAS  Google Scholar 

  • McCloskey DI (1973) Differences between the senses of movement and position shown by the effects of loading and vibration of muscles in man. Brain Res 63:119–131

    Article  Google Scholar 

  • McCloskey DI (1978) Kinesthetic sensibility. Physiol Rev 58:763–820

    PubMed  CAS  Google Scholar 

  • McGurk H, MacDonald J (1976) Hearing lips and seeing voices. Nature 264:746–748

    Article  PubMed  CAS  Google Scholar 

  • Mense S, Meyer H (1985) Different types of slowly conducting afferent units in cat skeletal muscle and tendon. J Physiol 363:403–417

    PubMed  CAS  Google Scholar 

  • Naito E, Ehrsson HH, Geyer S, Zilles K, Roland PE (1999) Illusory arm movements activate cortical motor areas: a positron emission tomography study. J Neurosci 19:6134–6144

    PubMed  CAS  Google Scholar 

  • Paillard J, Brouchon M. (1968) Active and passive movements in the calibration of position sense. In: Freedman AJ (eds) The neuropsychology of spatially oriented behavior. Dorsey Press, Homewood, pp 37–55

    Google Scholar 

  • Prochazka A (1996) Proprioceptive feedback and movement regulation. In: Rowell LB, Shepherd JT (eds) Handbook of physiology, Sect. 12, Exercise: regulation and integration of multiple systems. Oxford University Press, New York, pp 89–127

    Google Scholar 

  • Proske U, Schaible H-G, Schmidt RF (1988) Joint receptors and kinaesthesia. Exp Brain Res 72:219–224

    Article  PubMed  CAS  Google Scholar 

  • Radovanivic S, Korotkov A, Ljubisavljevic M, Lyskov E, Thunberg J, Kataeva G, Danko S, Roudas M, Pakhomov S, Medvedev S, Johansson H (2002) Comparison of brain activity during different types of proprioceptive inputs: a positron emission tomography study. Exp Brain Res 143:276–285

    Article  PubMed  Google Scholar 

  • Roll JP, Vedel JP (1982) Kinaesthetic roles of muscle afferents in man studied by tendon vibration and microneurography. Exp Brain Res 47:177–190

    Article  PubMed  CAS  Google Scholar 

  • Roll JP, Gilhodes JC, Tardy-Gervet MF (1980) Effets perceptifs et moteurs des vibrations musculaires chez l’homme normal: Mise en èvidence d’une rèsponse des muscles antagonistes. Arch Ital Biol 118:51–71

    PubMed  CAS  Google Scholar 

  • Roll JP, Vedel JP, Ribot E (1989) Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp Brain Res 76:213–222

    Article  PubMed  CAS  Google Scholar 

  • Sittig AC, Denier van der Gon JJ, Gielen CCAM (1985) Separate control of arm position and velocity demonstrated by vibration of muscle tendon in man. Exp Brain Res 60:445–453

    PubMed  CAS  Google Scholar 

  • Sittig AC, Denier van der Gon JJ, Gielen CCAM (1987) The contribution of afferent information on position and velocity to the control of slow and fast human forearm movements. Exp Brain Res 67:33–40

    Article  PubMed  CAS  Google Scholar 

  • Sommer J (1939) Synchronisierung motorischer Impulse und ihre Bedeutung für die neurophysiologische Forschung. Z ges Neurol Psychiat 172:500–530

    Article  Google Scholar 

  • Urbantschitsch V (1880) Über die Einfluss einer Sinneseregung auf die übrigen Sinnesempfindungen. Pflügers Archief für die desamte Physiologie des Menschen und der Tiere 42:155–179

    Google Scholar 

  • Vedel JP, Roll JP (1983) Muscle spindle contribution to the coding of motor activities in man. In: Neural coding of motor performance. Exp Brain Res (Suppl. 7), pp. 253–265

Download references

Acknowledgements

The authors gratefully acknowledge the National Institutes of Health for funding this project (AR31017). S.B. was a postdoctoral fellow of the Research Council, Katholieke Universitet Leuven, Belgium (PDM/99/121) and C.F-V. was a postdoctoral fellow of FAPESP, Brazil (97/129968-5).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. J. Cordo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cordo, P.J., Gurfinkel, V.S., Brumagne, S. et al. Effect of slow, small movement on the vibration-evoked kinesthetic illusion. Exp Brain Res 167, 324–334 (2005). https://doi.org/10.1007/s00221-005-0034-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-005-0034-x

Keywords

Navigation