Proprioception is not a single sensation but a group of sensations. It includes the sensations of position and movement of joints (loosely termed ‘joint position sense’ by neurologists), sensations of muscular force and effort, sensations related to the perceived timing of contractions, and sensations related to the body image. As well as this diversity in the various sensations making up proprioception, even for an individual component more than one mechanism can operate. From an evolutionary point of view this redundancy is not surprising: it ensures that crucial elements in the control of movement are not dependent on a single channel of information.
Clinicians frequently assess a patient's sensation of passive movement of a joint. If it is unimpaired, they then know that some peripheral receptors, their links to the spinal cord via peripheral nerves, and their ascending pathways to the thalamus and then to specialized regions of the cerebral cortex, are all intact. Controversy has dogged understanding of this aspect of proprioception, because researchers have often emphasized the role of one category of input and appeared to deny the role of other inputs. However, it is now clear that input from muscle, joint, and skin receptors can provide perceived signals that joints have moved, and in which direction.
Signals from the sensory endings within the main receptors in muscles, the muscle spindles, probably play an important role in signalling the direction of passive movements and their velocity. Muscle spindle endings respond to very small changes in muscle length, and the gain of their input can be affected by the specialized motor output from the spinal cord to the spindles, termed the fusimotor system. Specific signals from muscle spindle endings are interpreted centrally in the light of the fusimotor output to them, along with signals from antagonist muscles, joints, and nearby skin. Most joint receptors discharge towards the extreme end of a range of movement, while some local and more remote cutaneous receptors discharge as the skin is distorted by movement of nearby joints.
The force of a muscle contraction, and the apparent heaviness of weights actively lifted by the limb, are encoded by sensitive tension receptors (Golgi tendon organs). They are connected between the muscle fibres and intramuscular extensions of the tendon, and they respond to global forces generated actively by the muscle. However, a potent additional mechanism dominates judgements about force and heaviness: signals of motor command or effort are critical. An abnormal increase in motor command or effort can explain why weights lifted by fatigued or pathologically weakened muscles feel heavy despite the fact that their physical weight is unchanged. In an experimental situation subjects can distinguish between the signals of central command and those of peripheral force. However, this distinction is less obvious when lifting a heavy suitcase at an airport — it still seems to get heavier.
For the various sensations comprising proprioception, acuity is not necessarily identical at all joints of the body. As examples, detection of passive movements applied to the terminal joint of the big toe over a range of velocities is comparatively poor, while, for judgements of force, accuracy is comparatively high across a wide range of forces for the terminal joint of the thumb.
Rather like the judgements of force, the proprioceptive mechanisms that determine the perceived timing of muscle contractions have both a ‘peripheral’ and a ‘central’ component. Subjects can attend to either a central signal associated with the motor command to move, or one arising from muscle, joint, and skin receptors after the muscle contraction has begun. Clearly the former signal is generated without a peripheral input, because it arises before movement occurs. Furthermore, subjects can accurately attend to signals about the size and destination of motor commands, particularly those directed to the intrinsic muscles which move the fingers and thumb.
The importance of input from proprioceptors is highlighted when peripheral nerve damage (such as a severe sensory neuropathy), or damage within the brain (such as a stroke), eliminates sensations based on signals from specialized muscle, joint, and cutaneous receptors. When this occurs there is marked impairment of tasks requiring manipulative skill and the co-ordination of multiple muscle groups, such as walking. It also becomes difficult to sustain a steady muscle contraction. More restricted losses of proprioceptive inputs, such as those following surgical replacement of joints, produce only minor impairment to proprioception.
Gandevia, S. C. (1996). Kinesthesia: roles for afferent signals and motor commands. In Handbook on integration of motor, circulatory, respiratory and metabolic control during exercise, (ed. L. B. Rowell and J. T. Shepherd), pp. 128–72. American Physiological Society.
McCloskey, D. I. (1978). Kinesthetic sensibility. Physiological Review, 58, 763–820.
See also balance; joints; movement; sensory receptors; skeletal muscle.
"proprioception." The Oxford Companion to the Body. . Encyclopedia.com. (May 21, 2019). https://www.encyclopedia.com/medicine/encyclopedias-almanacs-transcripts-and-maps/proprioception
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