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Review
, 587 (Pt 17), 4139-46

The Kinaesthetic Senses

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Review

The Kinaesthetic Senses

Uwe Proske et al. J Physiol.

Abstract

This review of kinaesthesia, the senses of limb position and limb movement, has been prompted by recent new observations on the role of motor commands in position sense. They make it necessary to reassess the present-day views of the underlying neural mechanisms. Peripheral receptors which contribute to kinaesthesia are muscle spindles and skin stretch receptors. Joint receptors do not appear to play a major role at most joints. The evidence supports the existence of two separate senses, the sense of limb position and the sense of limb movement. Receptors such as muscle spindle primary endings are able to contribute to both senses. While limb position and movement can be signalled by both skin and muscle receptors, new evidence has shown that if limb muscles are contracting, an additional cue is provided by centrally generated motor command signals. Observations using neuroimaging techniques indicate the involvement of both the cerebellum and parietal cortex in a multi-sensory comparison, involving operation of a forward model between the feedback during a movement and its expected profile, based on past experience. Involvement of motor command signals in kinaesthesia has implications for interpretations of certain clinical conditions.

Figures

Figure 1
Figure 1. The technique of muscle conditioning
The two diagrams at the top show a human forearm with one flexor and one extensor muscle drawn in, the flexor being colour-coded. On the left, the arm is held flexed (dashed lines) and the flexors are contracted (conditioning flexed). Once the arm has relaxed it is moved to an intermediate angle (test). This leaves biceps and its spindles in a ‘taut’ state (red). When the arm is held extended (dashed lines) and elbow extensors are contracted (conditioning extended), moving the arm to the intermediate angle (test) leads to development of ‘slack’ in biceps and its spindles (blue). The lower diagram shows an instantaneous frequency display of the responses of a muscle spindle in the cat soleus muscle following conditioning of the muscle leaving the spindle taut (red) or slack (blue). Muscle conditioning leads to substantial changes in spindle discharge rates and that, in turn, leads to errors in forearm position sense. Redrawn, in part, from Wood et al. (1996).
Figure 4
Figure 4. Measuring position sense
Upper panel, apparatus used for position matching at the elbow joint. The experimenter places one arm at a set angle and the blindfolded subject matches its position with their other arm. The arms are supported by a pair of paddles which are hinged at a point aligned with the elbow joint and potentiometers at the hinge give the elbow angle. A weight can be attached under the paddle to load the arm. (Redrawn from Allen & Proske, 2006, with kind permission of Springer Science + Business Media.) Lower panel, apparatus used to measure position of the hand at the wrist. The fingers are held in full extension by a pair of plates which can be rotated through a range of angles. At each angle the subject indicates the perceived position of their hand by moving the pointer with their other hand. A nerve block can be effected by inflation of a cuff on the upper arm to produce ischaemic paralysis and anaesthesia of the hand. A similar cuff is used to restrict the distribution of a paralysing drug injected into the lower arm. From Smith et al. 2009.
Figure 2
Figure 2. Position-matching errors in the vertical plane
Values are means (±s.e.m.) for 12 subjects. Matching errors in the direction of extension are shown as positive. Dotted line, zero error. For this experiment both arms had been flexion conditioned before each matching trial. The four conditions for the reference arm were: supported by the experimenter, supported by the subject, supported by the subject with a 10% maximum voluntary contraction load added, and supported by the subject with a 25% load added. Despite one arm bearing an increasingly heavy load, matching accuracy remains unaffected. From Allen et al. (2007).
Figure 3
Figure 3. Change in perceived position of a phantom hand during flexion and extension
Left-hand panel, data before a total nerve block; right-hand panel, after the nerve block. Drawings at the top, when the relaxed hand was placed at each angular position, its perceived position is indicated by the black bar. Lower panel, perceived position of the relaxed hand (mean ±s.e.m.) at each of 6 angular positions (open triangles) and the perceived position during isometric efforts at 30% of maximum in the direction of flexion (filled circles) and the direction of extension (filled squares). Dashed line indicates accurate match. Before the nerve block, subjects are able to accurately indicate the position of the unseen hand. Isometric efforts produce only small errors. After the block, subjects are no longer able to indicate the position of the hand and efforts to move the hand produce large illusions of hand displacement. From Gandevia et al. (2006).

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