Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T18:37:18.422Z Has data issue: false hasContentIssue false
  • English
  • Français

Sensory feedback to the cerebral cortex during voluntary movement in man

Published online by Cambridge University Press:  04 February 2010

P. E. Roland
P. E. Roland
Affiliation:
Department of Clinical Physiology, Bispebjerg Hospital, Bispebjerg Bakke 23 DK-2400, NV, Copenhagen, Denmark
Get access Rights & Permissions [Opens in a new window]

Abstract

This article describes a series of experiments directed toward the following questions: (1) Do signals from musculotendinous receptors reach consciousness? (2) Does feed-forward information of muscular force and expected extent of voluntary movement exist? To answer these questions data from voluntary compression of springs and strain-gauge have been analysed in healthy young subjects and in patients with unilateral focal lesions of the cerebral hemispheres.

By successive elimination of information from other sources it was possible to verify that receptors in muscles and tendons do signal movement magnitude and muscular tension to the cerebral cortex, and that this information does indeed reach consciousness. There also exists a feed-forward mechanism signalling parameters of voluntary contraction. However, it is unclear whether peripheral, subcortical, or intracortical loops are directly involved. Perception of signals of muscular tension is abolished by lesions of the contralateral cortex near the central sulcus. It is possible that there exist separate cortical projection areas for kinaesthetic signals from muscles and from joints.

Keywords

consciousnessdiscriminationkinaesthesiamotor feedbackmuscle receptorsperceptionvoluntary movement
Type
Target Article
Information
Behavioral and Brain Sciences , Volume 1 , Issue 1 , March 1978 , pp. 129 - 147
Copyright
Copyright © Cambridge University Press 1978

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alnæs, , (1967) Static and dynamic properties of Golgi tendon organs in the anterior tibial and soleus muscles of the cat. Acta physiol. scand. 70:176–87.CrossRefGoogle Scholar
Bessou, P., Emonet-Denand, F, and Laporte, Y (1965) Motor fibres innervating extrafusal and intrafiisal muscle fibres in the cat. J. Physiol. 180:649–72.CrossRefGoogle ScholarPubMed
Bonde-Petersen, F, Gollnick, P. D., Hansen, T. I., Hulten, N., Knstensen, J. H., Secher, N., Secher, O. (1975) Glycogen depletion pattern in human muscle fiber during work under curanzation (d-tubocurarine). In: Metabolic adaption to prolonged physical exercise. Proceedings of the second international symposium on biochemistry of exercise, Magglingen, 1973, edited by Howald, H. and Poortmans, J. R.. Basel: Birkhauser Verlag 422–30.Google Scholar
Boyd, I. A., and Roberts, T. D. M. (1953) Proprioceptive discharges from stretch-receptors in the knee-joint of the cat. J. Physiol. 122:38–58.CrossRefGoogle ScholarPubMed
Brindley, G. S., and Merton, P. A. (1960) The absence of position sense in the human eye. J. Physiol. 153:127–30.CrossRefGoogle ScholarPubMed
Brown, M. C., Engberg, I., and Matthews, P. B. C. (1967) The relative sensitivity to vibration of muscle receptors of the cat. J. Physiol 192:773–800.CrossRefGoogle ScholarPubMed
Burgess, P. R, and Clark, F. J. (1969) Characteristics of knee joint receptors in the cat. J. Physiol. 203:317–35.CrossRefGoogle ScholarPubMed
Burke, D., Hagbart, K-E., Löfstedt, L., and Wallin, B. G. (1976a) The responses of human muscle spindle endings to vibration of noncontracting muscles. J. Physiol. 261:673–93. (1976b)Google ScholarPubMed
The responses of human muscle spindle endings to vibration during isometric contraction. J. Physiol 261:695–711.CrossRefGoogle Scholar
Campbell, E. J. M., Edwards, R. H. T, Hill, D. K., Jones, D A., and Sykes, M. K. (1976) Perception of effort during partial curanzation. J. Physiol 263.186P–187P.Google Scholar
Chambers, R. A., and Gilliat, R. W. (1954) The clinical assessment of postural sensation in the fingers. J. Physiol 123: 42 P.Google Scholar
Cheney, P D., and Preston, J. B. (1976) Effects of fusimotor stimulation on dynamic and position sensitivities of spindle afferents in the primate. J Neurophysiol. 39:21–30.CrossRefGoogle ScholarPubMed
Clark, F J., and Burgess, P. R. (1975) Slowly adapting receptors in cat knee ioint: can they signal joint angle? J. Neurophysiol 38:1448–63.CrossRefGoogle Scholar
Cohen, E. N., Hood, N., and Golling, R. (1968) Use of whole-body autoradiography for determination of uptake and distribution of labeled muscle relaxants in the cat. Anesthesiology, 29:987–93.CrossRefGoogle Scholar
Cohen, L A. (1958) Contributions of tactile musculotendineous and joint mechanisms to position sense in human shoulder. J. Neurophysiol 21:563–68.CrossRefGoogle Scholar
(1958a) Analysis of position sense in human shoulder, J. Neurophysiol. 21:550–62.CrossRefGoogle Scholar
Coulter, J. D., and Tones, E. G. (1977) Differential distribution of corticospinal projections from individual cytoarchitectonic fields in the monkey. Brain Res. 129:335–40.CrossRefGoogle ScholarPubMed
Cross, M. J., and McCloskey, D I. (1973) Position sense following surgical removal of joints in man. Brain Res. 55:443–45.CrossRefGoogle ScholarPubMed
Dijkstra, S., and van der Gon, J.J. D. (1973) An analog computer study of fast, isolated movements Kybernetik 12:102–10.CrossRefGoogle ScholarPubMed
Duffy, F H., and Burchfiel, J. L. (1971) Somatosensory system: Organizational hierarchy from single units in monkey area 5. Science 172:273–75.CrossRefGoogle ScholarPubMed
Dyhre-Poulsen, P., and Djørup, A. (1976) The effect of sensory input on reflex load compensation Acta Physiol. Scand. suppl. 440:58.Google Scholar
Eklund, G. (1972) Position sense and state of contraction; the effects of vibration J. Neurol. Neurosurg. Psychiat. 35:606–11.CrossRefGoogle Scholar
Emonet-Denand, F., and Houk, J. (1968) Étude comparative de la curansation des synapses neuromusculaires des fibres fusimotrices dynamiques et statiques, chez le chat.J. Physiol. 60:367–72Google Scholar
Evarts, E. V. (1966) Pyramidal tract activity associated with a conditioned hand movement in the monkey.J. Neurophysiol. 29:1011–27. (1968)CrossRefGoogle ScholarPubMed
Relation of pyramidal tract activity to force exerted during voluntary movement.J Neurophysiol. 31:14–27.Google Scholar
(1973) Motor cortex reflexes associated with learned movements. Science 179: 501–3.CrossRefGoogle Scholar
and Tanji, J. (1976) Effects of instruction on pertubation-evoked activity of motor cortex neurons in monkey.J. Neurophysiol. 39:1069–80.Google Scholar
von Frey, M. (1914) Studien ŭber den Kraftsinn.Z. Biol. 63:129–154. (1915)Google Scholar
Die Vergleichung von Gewichten mit Hilfe des Kraftsinns. Z.Biol. 65:203–24.Google Scholar
Freyschuss, U. (1970) Cardiovascular adjustment to somatomotor activation. Acta Physiol. Scand. suppl. 342:63.Google ScholarPubMed
Gandevia, S. C, and McCloskey, D. I. (1976) Joint sense, muscle sense and their combination as position sense, measured at the distal interphalangeal joint of the middle finger.J. Physiol. 260:387–407.(1977a)CrossRefGoogle ScholarPubMed
Sensations of heaviness. Brain. In press.(1977b)Google Scholar
Effects of related sensory inputs on motor performances in man studied through changes in perceived heaviness.J. Physiol. In press.(1977c)Google Scholar
Changes in motor commands, as shown by changes in perceived heaviness, during partial curarization and peripheral anaesthesia in man.J. Physiol. In press.Google Scholar
Gardner, E. (1967) Spinal cord and brain stem pathways for afferents from joints. In: Myotatic, Kinaesthetic and Vestibular mechanisms, edited by de Reuck, A. V. S. and Knight, J.. London: Churchill. 56–76.Google Scholar
Gelfan, S., and Carter, S (1967) Muscle sense in man. Exp. Neurol. 18:469–73.CrossRefGoogle ScholarPubMed
A., Goldscheider (1898) Gesammelte Abhandlungen II. Physiologic des Muskelsinnes. Leipzig: J. A. Barth.Google Scholar
Goodwin, G. M., McCloskey, D. I., and Matthews, P B. C (1972) The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. Brain 95:705–48.CrossRefGoogle ScholarPubMed
Goodwin, G. M., McCloskey, D. I., and Mitchell, J. H. (1972) Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension J Physiol. 226:173–90.CrossRefGoogle ScholarPubMed
Granit, R.,Homma, S., and Matthews, P. B C. (1959) Prolonged changes in the discharge of mammalian muscle spindles following tendon taps or muscle twitches. Acta Physiol. Scand, 46:185–93.(1972)CrossRefGoogle ScholarPubMed
Constant errors in the execution and appreciation of movement. Brain 95:649–60.Google Scholar
Grigg, P. (1975) Mechanical factors influencing response of joint afferent neurons from cat knee.J Neurophysiol. 38:1473–88.CrossRefGoogle ScholarPubMed
Grillner, S. (1973) On the spinal generation of locomotion. In: Sensory organization of movements, edited by Batueu., A. S. Leningrad.(1975)Google Scholar
Locomotion in vertebrates: Central mechanisms and reflex interaction. Physiol. Rev. 55:247–304.CrossRefGoogle Scholar
Hallet, M., Shahani, B. T., and Young, R. R. (1975) EMG analysis of stereotyped voluntary movements in man.J Neurol. Neurosurg. Psychiat. 38:1154–62.Google Scholar
Hammond, P. H. (1955) Involuntary activity in biceps following the sudden application of velocity to the abducted forearm.J. Physiol. 127:23P–25P.(1956)Google Scholar
The influence of prior instruction to the subject on an apparently involuntary neuromuscular response.J. Physiol. 132:17P–18P.Google Scholar
Hill, A. V. (1922) The maximum work and mechanical efficiency of human muscles, and their most economical speed.J. Physiol. 56:19–41.CrossRefGoogle ScholarPubMed
Hinsey, J. C., Ranson, S. W., and McMattin, R. F. (1930) The role of the hypothalamus and mesencephalon in locomotion. Arch. Neurol. Psychiat. 23:1–43.CrossRefGoogle Scholar
von Hoist, E. (1954) Relations between the central nervous system and the peripheral organs. Brit.J. Anim. Behavn. 2:89–94.CrossRefGoogle Scholar
Hore, J., Presto, J. B., Durkovic, R. G., and Cheneu, P. D. (1976) Response of cortical neurons (areas 3a and 4) to ramp stretch of hindlimb muscles in the baboon J. Neurophysiol 39:484–501.CrossRefGoogle ScholarPubMed
Houk, J., and Henneman, E (1967) Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat.J. Neurophysiol 30:466–81Google ScholarPubMed
Katz, D. (1925) DerAufbau derTastwelt Leipzig: Ambrosius Barth.Google Scholar
Kennedy, D. (1973) Control of motor output. In: Control of posture and locomotion, edited by Stein, R. B., Pearson, K. G., Smith, R. S., and B., J.Redford New York: Plenum Press 429–36.Google Scholar
Krogh, A., and Lindhard, J. (1913) The regulation of respiration and circulation during the initial stages of muscular work.J Physiol. 47:112–36CrossRefGoogle Scholar
Landgren, S, and Silfvenius, H. (1969) Projection to the cerebral cortex of group I muscle afferents from the cat's hindlimb.J. Physiol. 200:353–72.CrossRefGoogle Scholar
Marsden, C. D, Merton, P A., Morton, H B (1971) Servo action and stietch reflex in human muscle and its apparent dependence on peripheral sensation.J Physiol 216:21–22 P(1977)Google ScholarPubMed
The sensory mechanism of servo action in human muscle, J Physiol 265:521–35Google Scholar
Matthews, B. H. C (1933) Nerve endings in mammalian muscle.J. Physiol. 78:1–53.(1964)CrossRefGoogle ScholarPubMed
Muscle spindles and their motor control. Physiol. Rev. 44:219–88.Google Scholar
Matthews, P B. C. (1972) Mammalian muscle receptors and their central actions London: Arnold. 630andGoogle Scholar
Simmonds, A(1974) Sensations of finger movement elicited by pulling upon flexor tendons in man J. Physiol. 239:27–28 P.Google Scholar
McCloskey, D. I., Ebeling, P., and Goodwin, G. M. (1974) Estimation of weights and tensions and apparent involvement of a “sense of effort” Exp Neurol 42:220–32CrossRefGoogle ScholarPubMed
McCloskey, D I, and Torda, T A. G (1975) Corollary motor discharges and kinaesthesia Brain Res 100:467–70CrossRefGoogle ScholarPubMed
Merton, P. A. (1951) The silent period in a muscle of the human hand.J Physiol. 114:183–98(1953)CrossRefGoogle Scholar
Speculations on the servo-control of movement In: The Spinal Cord, edited by Wolstenholme, G E W.London: Churchill 247–55.(1964a)Google Scholar
Human position sense and sense of effort. In: Homeostasis and feedback mechanisms, edited by Hughes, G. M.. Symp. Soc. Exper. Biol 18:387–400Google Scholar
(1964b) Absence of conscious position sense in the human eyes. In: The Oculomotor system, edited by Bender, M.New York: Harper and Row 314–20.(1970)Google Scholar
The sense of effort In: Breathing Heving-Breuer Centenary Symposium, edited by Porter, RLondon: Churchill 207–11(1972)Google Scholar
How we control the contraction on our muscles. Sci Am., 226:530–38Google Scholar
Millar, J (1972) Joint afferent discharge following muscle contraction in the absence of joint movement J Physiol 226:72 PGoogle ScholarPubMed
Mountcastle, V. B, and Darian-Smith, I (1968) Neural mechanisms in somesthesia. In: Medical Physiology, edited by Mountcastle, V. B., vol 2 Saint Louis: Mosby, 1372–1423Google Scholar
Mountcastle, V. B, and Powell, T P. S. (1959) Central nervous mechanisms subserving position sense and kinaesthesis Bull Johns Hopkins Hosp. 105:173–200Google Scholar
Phillips, C G. (1966) Changing concepts of the precentral motor area. In: Brain and conscious experience, edited by Eccles., J. C.Heidelberg:Springer 389–421(1969)Google Scholar
The Ferrier Lecture, 1968 Motor apparatus of the baboon's hand Proc. R Soc. B, 173:141–74Google Scholar
Phillips, C G., Powell, T P S., and Wiesendanger, M (1971) Projection from low- threshold muscle afferents of hand and forearm to area 3a of baboon's cortex J Physiol 217:419–46.CrossRefGoogle ScholarPubMed
Powell, T. P S., and Mountcastle, V. B. (1959) Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: A correlation of findings obtained in a single unit analysis with cytoarchitecture. Bull Johns Hopkins Hosp 105:133–62.Google Scholar
Provins, K A (1958) The effect of peripheral nerve block on the appreciation and execution of finger movements J Physiol. 143:55–67.CrossRefGoogle ScholarPubMed
Renquist, Y (1927) ŭber den Bewegungswahrnehmungen zugrunde liegenden Reize Skan Arch, Physiol. 50:52–96.CrossRefGoogle Scholar
Roland, P. E. (1973) Lack of appreciation of compressibility, adynamaesthesia and akinaesthesia.J. Neurol. Sci. 20:51–61.(1975)CrossRefGoogle ScholarPubMed
Do muscular receptors in man evoke sensations of tension and kinaesthesia? Brain Res. 99:162–65.(1976)Google Scholar
Astereognosis. Arch.Neurol. 33: 543–50.(1978)Google Scholar
Impairment of kinaesthesia and sensations of tension after focal cerebral lesions in man. (Submitted for publication).Google Scholar
Roland, P. E., and Ladegaard-Pedersen, H. (1977) A quantitative analysis of sensations of tension and kinaesthesia in man. Evidence for a peripherally originating muscular sense and for a sense of effort. Brain. 100. In press.Google Scholar
Rose, J. E., and Mountcastle, V. B. (1960) Touch and kinaesthesia. In: Handbook of Physiology. Section 1, Vol. l, Neurophysiology, edited by Field, J., Washington, D.C., Amer. Physiol. Soc. 387–427.Google Scholar
Shik, M. L, Severin, F. V., and Orlovsky, G. N. (1966) Control of walking and running by means of electrical stimulation of the mid-brain. Biofizika, 11 659–66. (Translated from the Russian.)Google Scholar
Skoglund, S. (1956) Anatomical and physiological studies of knee joint innervation in the cat. Acta. Physiol. Scand. 36: Suppl. 124. (1973)Google ScholarPubMed
Joint receptors and kinaesthesis. In: Handbook of Sensory Physiology Vol. II: Somatosensory System, edited by Iggo, A.. Heidelberg: Springer. 111–36.Google Scholar
Soechting, J. F. (1973) Modeling of a simple motor task in man: Motor output dependence on sensory input. Kybernetik 14:25–34.CrossRefGoogle ScholarPubMed
Sperry, R. W. (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion.J Comp Physiol. Psychol. 43:482–89.CrossRefGoogle ScholarPubMed
Swett, J. E., and Bourassa, C. M. (1967) Comparison of sensory discrimination thresholds with muscle and cutaneous nerve volleys in the cat.J. Neurophysiol. 30: 530–45. and Inoue S. (1964)CrossRefGoogle ScholarPubMed
Effects of cutaneous and muscle sensory nerve volleys in awake cats: A study of perception. Science 145:1071–73.Google Scholar
Talairach, J., Szikla, G., Tournoux, P., Prossalentis, A., Bordas-Ferrer, M., Covello, L, Iacob, M., and Mempel, E. (1967) Atlas d'anatomie stereotaxique du telencephale Paris: Masson et Cie.Google Scholar
Tanji, J., and Evarts, E. V. (1976) Anticipatory activity of motor cortex neurons in relation to direction of an intended movement.J. Neurophysiol. 39:1062–66.CrossRefGoogle ScholarPubMed
Taub, E., and Berman, A. J. (1968) Movement and learning in the absence of sensory feedback. In: The neuropsychology of spatially oriented behavior, edited by Freeman, S. J.. Homewood, Illinois: Dorsey, 173–92.Google Scholar
Taub, E., Ellman, S. J., and Berman, A. J. (1966) Deafferentiation in monkeys: Effect on conditioned grasp response. Science 151:593–94.CrossRefGoogle Scholar
Taub, E, Perrella, P. N., and Barro, G (1972) Behavioral development in monkeys following bilateral forelimb deafferentation on the first day of life. Trans. Am.Neurol.Ass. 97: 101–4.(1973)Google Scholar
Behavioral development after forelimb deafferentiation on day of birth in monkeys with and without blinding. Science 181:959–60.Google Scholar
Ten Cate, J. and van Herk, A. W. H. (1933) Beobachtungen an Kaninchen nach exstirpationen in Neopallium. Arch. Neel.Physiol. 18:15–23.Google Scholar
Vallbo, A. B. (1970) Slowly adapting muscle receptors in man. Acta. Physiol.Scand. 78: 315–33.(1971)CrossRefGoogle ScholarPubMed
Muscle spindle response at the onset of isometric voluntary contractions in man. Time differences between fusimotor and skeletomotor effects.J. Physiol. 318: 405–31.(1973)Google Scholar
The significance of intramuscular receptors in load compensation during voluntary contractions in man. In: Control of posture and locomotion, edited by Stein, R. B., Pearson, K. G., Smith, R. S., and B., J.Redford New York: Plenum Press. 211–26.(1974)Google Scholar
Human Muscle Spindle Discharge during Isometric Voluntary Contractions. Amplitude Relations between Spindle Frequency and Torque. Acta. Physiol. Scand. 90:319–36.Google Scholar
Viviani, P., and Terzuolo, C A. (1973) Modeling of a sample motor task in man: Intentional arrest of an ongoing movement. Kybernetik 14:35–62.CrossRefGoogle Scholar
Wachholder, K., and Altenburger, H. (1926) Beiträge zur Physiologie der willkürlichen Bewegung. 10. Einzelbewegungen. Pflügers Arch. Ges. Physiol 214:642–61.Google Scholar
Werner, G, and Mountcastle, V. B (1963) The variability of central neural activity in a sensory system, and its implications for the central reflexion of sensory events J. Neurophysiol. 26:958–77.CrossRefGoogle Scholar