Proprioceptive Sensory Feedback

Abstract

Proprioceptors are sensors that provide information about orientation of the body relative to the body's orientation with respect to gravity, movement of the body relative to the external medium and movements and forces in localised regions of the body. Muscle spindles are primarily responsible for position and movement sense, Golgi tendon organs provide the sense of force and the vestibular system provides the sense of balance. Feedback from proprioceptors feedback is essential for the accurate execution of movement execution. For voluntary limb movements in primates, proprioceptive feedback can regulate the generation of motor command by correcting errors using negative feedback loops; providing timing cues about an ongoing movement to initiate commands required at a later time within a movement sequence; and by providing signals used in the planning of movements by providing information about starting limb position to set parameters of feedforward commands. Proprioceptive feedback is also required to modify motor commands slowly in response to alterations in the biomechanical properties of the limbs.

Key Concepts:

  • Proprioception is a peripherally derived kinaesthetic sense.

  • Position and movement sense is provided by muscle spindles.

  • Muscle tension is sensed by Golgi tendon organs.

  • The centrally derived sense of effort gives information about force and heaviness of objects.

  • Proprioceptors project to the motor cortex via the dorsal columns and to the cerebellum via spinocerebellar tracts.

  • Proprioceptive information is used in the spinal regulation of rhythmic movements.

Keywords: proprioceptors; muscle receptors; motor control; motor programme; reflexes; voluntary movement; walking; locust flight

Figure 1.

Feedback from muscle spindles and Golgi tendon organs controls stepping of the hind leg of the cat. (a) Simplified drawings of mammalian muscle spindles and (b) their firing properties in response to various stimuli. (c) Simplified drawings of a Golgi tendon organ and (d) its firing properties. (e) An intracellular recording from an ankle extensor motoneuron demonstrating the reflex reversal of group Ib afferents. At rest, 200 Hz stimulation of group Ib afferents inhibits medial gastrocnemius muscle activity. During locomotion, the same stimulation enhances medial gastrocnemius muscle activity. See text for details. Panels (a) and (b) are modified from Matthews with permission from the American Physiological Society. Panel (c) Modified with permission from Jami . Panel (e) Modified with permission from Pearson et al..

Figure 2.

Proprioceptive feedback controls the timing of motor activity in the flight system of the locust. (a) Removal of wing proprioceptors (deafferented) reduces wingbeat frequency and shortens the period of flight in response to a constant wind stimulus. The two sets of data (intact and deafferented) are from the same animal. Wingbeat frequency was determined from electrical recordings of muscle activity, whereas the animal flew in a wind stream (inset) (from Pearson and Ramirez ). (b) Schematic diagram showing the organisation of feedback pathways from tegulae and stretch receptors that control wingbeat frequency. Phasic signals from the tegulae (activated by wing depression) initiates activity in elevator (Elev.) motor neurons via elevator interneurons (EINs in shaded box) in the central rhythm generator and via interneurons (int.) that are not elements of the central rhythm generator. Feedback from the stretch receptors (activated by wing elevation) is timed to antagonise the hyperpolarisation in depressor interneurons (DINs in shaded box) in the central rhythm generator that excite depressor (Dep.) motor neurons. This action is delayed (D) to occur on the cycle following the wing elevation that activates the stretch receptors. Adapted from Pearson and Ramirez .

Figure 3.

Schematic diagram showing the organisation of feedback pathways from muscle spindles (group Ia and II afferents) and Golgi tendon organs (group Ib afferents) that control the timing and magnitude of activity in extensor (Ext.) and flexor (Flex.) motor neurons during stepping. The central rhythm generator (shaded box) is assumed to consist of mutual inhibiting extensor (E) and flexor (F) half‐centres. See text for details.

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References

Asanuma H and Arissian K (1984) Experiments on functional role of peripheral input to motor cortex during voluntary movements in the monkey. Journal of Neurophysiology 52: 212–227.

Bastian HC (1887) The ‘muscular sense’: its nature and cortical localisation. Brain 10: 1–89.

Cordo P, Bevan L, Gurfinkel V et al. (1995) Proprioceptive coordination of discrete movement sequences: mechanism and generality. Canadian Journal of Physiology and Pharmacology 73: 305–315.

Ekerot CF, Larson B and Oscarsson O (1979) Information carried by the spinocerebellar paths. Progress in Brain Research 50: 79–90.

Favorov O, Sakamoto T and Asanuma H (1988) Functional role of corticoperipheral loop circuits during voluntary movements in the monkey: a preferential bias theory. Journal of Neuroscience 8: 3266–3277.

Goodwin GM, McCloskey DI and Matthews PB (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: 705–748.

Grey MJ, Mazzaro N, Nielsen JB and Sinkjaer T (2004) Ankle extensor proprioceptors contribute to the enhancement of the soleus EMG during the stance phase of human walking. Canadian Journal of Physiology and Pharmacology 82: 610–616.

Grey MJ, Nielsen JB, Mazzaro N and Sinkjaer T (2007) Positive force feedback in human walking. Journal of Physiology 581: 99–105.

von Holst E and Mittelstaedt H (1950) Das Reafferenzprincip. Naturzvissenschaften 37: 464–476.

Jami L (1992) Golgi tendon organs in mammalian skeletal muscle: functional properties and central actions. Physiological Reviews 72: 623–666.

af Klint R, Mazzaro N, Nielsen JB, Sinkjaer T and Grey MJ (2010) Load rather than length sensitive feedback contributes to soleus muscle activity during human treadmill walking. Journal of Neurophysiology 103: 2747–2756.

Matthews PBC (1964) Muscle spindles and their motor control. Physiological Reviews 44: 219–288.

Mill PJ (1976) Structure and Function of Proprioceptors in the Invertebrates. London: Chapman and Hall.

Morita H, Petersen N, Christensen LO, Sinkjaer T and Nielsen J (1998) Sensitivity of H‐reflexes and stretch reflexes to presynaptic inhibition in humans. Journal of Neurophysiology 80: 610–620.

Pearson KG, Misiaszek JE and Foud K (1998) Enhancement and resetting of locomotor activity by muscle afferents. Annals of the New York Academy of Sciences 860: 203–215.

Pearson KG and Ramirez JM (1997) Sensory modulation of pattern‐generating circuits. In: Stein PSG, Grillner S, Selverston AI and Stuart DG (eds) Neurons, Networks, and Motor Behavior, pp. 225–236. Cambridge, MA: MIT Press.

Petersen N, Christensen LO, Morita H, Sinkjaer T and Nielsen J (1998) Evidence that a transcortical pathway contributes to stretch reflexes in the tibialis anterior muscle in man. Journal of Physiology 512: 267–276.

Prochazka A (1996) Proprioceptive feedback and movement regulation. In: Rowell L and Sheperd JT (eds) Handbook of Physiology. Section 12. Regulation and Integration of Multiple Systems, pp. 89–127. New York: American Physiological Society.

Prochazka A, Hulliger M, Zangger P and Appenteng K (1985) ‘Fusimotor set’: new evidence for alpha‐independent control of gamma‐motoneurones during movement in the awake cat. Brain Research 339: 136–140.

Proske U (2006) Kinesthesia: the role of muscle receptors. Muscle Nerve 34: 545–558.

Roll JP and Vedel JP (1982) Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography. Experimental Brain Research 47: 177–190.

Rothwell JC, Traub MM, Day BL et al. (1982) Manual motor performance in a deafferented man. Brain 105: 515–542.

Sainburg RL, Ghilardi MF, Poizner H and Ghez C (1995) Control of limb dynamics in normal subjects and patients without proprioception. Journal of Neurophysiology 73: 820–835.

Sinkjaer T, Andersen JB, Ladouceur M, Christensen LO and Nielsen JB (2000) Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man. Journal of Physiology 523: 817–827.

Sherrington CS (1906) On the proprioceptive system, especially in its reflex aspects. Brain 29: 467–482.

Sperry RW (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. Journal of Computational Physiology and Psychology 43: 482–489.

Zuur AT, Christensen MS, Sinkjaer T, Grey MJ and Nielsen JB (2009) Tibialis anterior stretch reflex in early stance is suppressed by repetitive transcranial magnetic stimulation. Journal of Physiology 587: 1669–1676.

Further Reading

Barnes WJP and Gladden MH (1985) Feedback and Motor Control in Invertebrates and Vertebrates. London: Croom Helm.

Boyd IA and Gladden M (1985) The Muscle Spindle. London: Macmillan.

Cole J (1995) Pride and a Daily Marathon. Cambridge, MA: MIT Press.

Donaldson IM (2000) The functions of the proprioceptors of the eye muscles. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355: 1685–1754.

Donelan JM and Pearson KG (2004) Contribution of sensory feedback to ongoing ankle extensor activity during the stance phase of walking. Canadian Journal of Physiology and Pharmacology 82: 589–598.

Gandevia SC and Burke D (1992) Does the nervous system depend on kinesthetic information to control natural limb movement? Behavioral and Brain Sciences 15: 614–632.

Gandevia SC, McCloskey DI and Burke D (1992) Kinaesthetic signals and muscle contraction. Trends in Neurosciences 15: 62–66.

Ghez C and Sainburg R (1995) Proprioceptive control of interjoint coordination. Canadian Journal of Physiology and Pharmacology 73: 273–284.

Gordon J, Ghilardi MF and Ghez C (1995) Impairments of reaching movements in patients without proprioception. I. Spatial errors. Journal of Neurophysiology 73: 347–360.

Johansson RS and Westling G (1987) Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip. Experimental Brain Research 66: 141–154.

Kawato M (1999) Internal models for motor control and trajectory planning. Current Opinion in Neurobiology 9: 718–720.

Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Annual Review of Neuroscience 16: 265–297.

Pearson KG (1995) Proprioceptive regulation of locomotion. Current Opinion in Neurobiology 5: 786–791.

Pearson KG (2008) Role of sensory feedback in the control of stance duration in walking cats. Brain Research Reviews 57: 222–227.

Proske U and Gandevia SC (2009) The kinaesthetic senses. Journal of Physiology 587: 4139–4146.

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How to Cite close
Grey, MJ(Oct 2010) Proprioceptive Sensory Feedback. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000071.pub2]