Reception of internal mechanical stimuli
Some proprioceptors (internal receptors) for mechanical stimuli provide information about posture and movements of parts of the body relative to each other; others contribute to an undisturbed course of coordinated muscular actions (e.g., in locomotion). Best known from studies of vertebrates and arthropods, some are tonic proprioceptors (serving to maintain muscle tone in posture); others are of the phasic type (serving movement); still others have a mixed phasic-tonic character. In principle, proprioceptors can be stimulated adequately by pressure or stretching during active movements of the animal (reafferent stimulation) as well as through passive external pushing and pulling (exafferent stimulation). One passive factor, particularly in land-inhabiting animals, is gravity as it acts on bodily tissues or organs. Proprioceptors thus not only serve reflex adjustments in posture and relatively automatic movements of parts of the body with respect to each other (as in driving an automobile), but they also provide gravitational information about the positions of limbs or of the whole body in space. To the extent that they are gravity detectors, these sensory structures are properly called external receptors (exteroceptors instead of proprioceptors). For receptors that are diffusely located within the body, a clean distinction between proprioceptive and possible exteroceptive function (gravity reception) is experimentally practicable only under conditions of weightlessness, as in space travel.
Vertebrates
Muscle spindles
Well-known proprioceptors of all the four-limbed vertebrates studied are the muscle spindles occurring in the skeletal (striate) muscles; fish muscles show structurally simpler but functionally comparable receptors. Each muscle spindle in mammals consists of a few slender, specialized (intrafusal) muscle fibres that are surrounded by a sheath of connective tissue filled with lymph fluid. The muscle spindle itself is surrounded by and arranged parallel to the ordinary (extrafusal) muscle fibres. Each intrafusal fibre consists of contractile (motor) parts at both ends and a noncontractile sensory midsection that serves as a receptor for stretch (changes of length and tension). There is double (primary and secondary) sensory innervation in mammals, but the secondary endings are lacking in lower vertebrates. Even when the animal is at rest, both types of endings are active (under the tension of normal muscle tonus). Additional stretch (lengthening) of the intrafusal midsection increases the nerve impulse frequency, and relaxation (shortening) causes a decrease. The primary (phasic-tonic) ending responds quickly; responses of the secondary (tonic) endings are slower.
The length of the muscle spindle as a whole varies with the contraction phase and the length of the muscle to which it belongs. The length of the sensory midsection, however, may change more or less independently because its motor nerve endings function apart from the innervation of the extrafusal muscle fibres. Thus the ratio of extrafusal–intrafusal contraction determines whether or not a change of length in the midsection will occur during muscle activity. There are reasons to suppose that midsection stretch remains more or less unchanged during self-initiated (“voluntary”) movements; reafferent stimulation of muscle spindles would be avoided in this way. But as soon as an unexpected (exafferent) stretch of a muscle occurs—for example, when a leg pushes against an obstacle during locomotion—the midsections stretch to produce an increase of impulse frequency. This neural activity elicits a compensatory reflex contraction of the stretched muscle, as in the knee jerk during medical examinations: a blow beneath the kneecap causes stretch of a thigh muscle, stimulation of its muscle spindles, and a compensatory jerking contraction of the same muscle.
Tendon organs
Branched nerve endings on vertebrate tendons (not far from their point of attachment to muscle) also respond to stretch; however, they are decidedly less sensitive than are muscle spindles. These tendon organs produce no impulses under the stretch of normal, resting muscle tonus. Neither is there a mechanism preventing reafferent stimulation of tendon organs, nor does it make any difference whether the stretch is brought about by active muscle contraction or passively following external influence. In both cases tendon receptors respond according to the intensity of the stretch; their response causes relaxation of the attached muscle and may serve (among other functions) to prevent anatomical damage.
Human awareness of posture and movement of parts of the body with respect to each other (kinesthetic sensations) is attributable neither to muscle spindles nor to tendon organs. The sensations are based on stimulation of sensory nerve endings of various types at the joint capsules and of stretch receptors in the skin. There are also mechanoreceptors in the walls of some blood vessels (e.g., in the aorta and the carotid sinus); these are sensitive to blood-pressure changes and play a regulatory role in the circulatory system.
Invertebrates
Among invertebrates, the arthropods exhibit the most readily distinguished proprioceptors, called muscle-receptor organs and chordotonal proprioceptors. Both types of structure occur in crustaceans as well as in insects. Adequate stimuli are variations in length and tension (stretch).
Muscle receptor organs
Although they structurally and functionally resemble the muscle spindles of vertebrates, arthropod muscle receptor organs are always situated outside of the muscles proper. Numerous branches of multipolar primary nerve cells are connected with the noncontractile midsection of specialized muscle fibres, both ends of which are contractile and have an efferent (motor) innervation. In crustaceans, the muscle receptor organ contains two elements: a slowly contracting, nonadapting tonic fibre and a quickly contracting, rapidly adapting phasic element.
Chordotonal proprioceptors
Widely distributed among arthropods, chordotonal receptor organs are thin, elastic, innervated strands of connective tissue, stretched between adjacent segments of the body or of leg joints. The sensory endings of a few bipolar primary nerve cells, each provided with a spiny sensillum (scolopidium), are attached to the strand. Chordotonal proprioceptor organs generate neural impulses that show them to contain both phasic movement receptors and tonic pressure receptors; sometimes two varieties of each. Thus there are receptors that selectively respond only during flexion, only in the flexed position, only during stretch, or only in the stretched state of the given strand. Several kinds of insects, apart from their clearly proprioceptive-chordotonal functions, have other chordotonal elements that serve as typical exteroceptors. Sense organs of this type (tympanic and subgenual organs in legs, Johnston’s organs in the antennae) may function in the reception of sound waves, of vibrations in the ground, or of other external mechanical stimuli. Many insects also have a special type of chordotonal-proprioceptor structure (campaniform sensilla) not found in crustaceans. Sensory endings of primary nerve cells are connected with thin, dome-shaped (campaniform) spots on the exoskeleton. These campaniform sensilla respond to external stimuli such as local tensions and deformations of the body surface. They function in the regulation of such movements as the beating of wings in locusts. Similarly functioning proprioceptors (lyriform organs) are also observed among spiders.
In insects, body posture and movements of individual body parts with respect to each other can be detected through groups of external tactile hairs implanted near the joints between adjacent skeletal elements. Some function as rotation receptors or exteroceptors to detect the direction of gravity.
Among other invertebrates, octopuses clearly exhibit proprioceptive abilities. These animals, however, seem unable to integrate proprioceptive data in the central nervous system with other sensory information in learning. Thus, an octopus readily can be taught to discriminate between two small cylindrical objects (both provided with longitudinal ribs) if the ribs on one of them are somewhat coarser than those on the other. But the animal cannot learn to distinguish between cylinders of the same size if the ribs are equally coarse and if they are longitudinal on one and transverse in the other; nor can it learn to discriminate between small objects of different form or different weight. This indicates that an octopus cannot learn any discrimination that depends on sensory information about the position of the arms and suckers making contact.