Termination patterns of identified group II and III afferent fibres from deep tissues in the spinal cord of the cat

Abstract

In chloralose-anaesthetized cats, the impulse activity of single afferent fibres supplying receptors in the deep tissues of the hindlimb (fasciae, muscles, ligaments, joint capsules) was recorded using micropipettes filled with a solution of horseradish peroxidase. Only myelinated fibres with conduction velocities up to 40 m/s (Group III and Group II units) were studied, i.e. fast conducting afferent fibres from muscle spindles and tendon organs were excluded. The fibres were functionally characterized with the use of mechanical stimuli such as local pressure and joint movements. The results show that a relationship exists between the functional properties of a given afferent unit and the location of its terminals in the spinal cord. Since the conduction velocity and hence the diameter of the fibres was similar in all the units studied, these factors appear not to be of importance for determining the pattern of spinal termination. Out of 84 units, 42 were classified as high-threshold mechanosensitive, 26 as low-threshold mechanosensitive, and 16 as secondary endings from muscle spindles. Following physiological identification the fibres were ionophoretically injected with horseradish peroxidase and their trajectory in the white and gray matter of the spinal cord visualized histologically with diaminobenzidine. High-threshold mechanosensitive units took a lateral course in the posterior funiculus and usually did not bifurcate. They exhibited two different patterns of spinal termination, one being characterized by terminal arborizations in both lamina I and deeper laminae (mostly IV/V), the other one by an exclusive projection to lamina I. Low-threshold mechanosensitive units often showed a bifurcation in the posterior funiculus and did not have a uniform termination pattern. The main areas of termination were lamina II and laminae IV–VI. The slowly conducting secondary endings from muscle spindles projected mainly to laminae VI and VII with additional collaterals entering the ventral horn. They thus had a termination pattern similar to that reported for fast conducting afferent fibres (above 50 m/s) from muscle spindle secondary endings. With the exception of one high-threshold mechanosensitive unit none of the stained fibres possessed terminal arborization and boutons in lamina III. It is concluded that different types of Group II and III primary afferent fibres from deep tissues exhibit different patterns of spinal termination. The heavy projections of high-threshold mechanosensitive (presumably nociceptive) units to lamina I and laminae IV/V—i.e. to layers which are known to contain cells of origin of ascending nociceptive tracts—may indicate that a monosynaptic pathway for deep pain exists at the spinal level. Since lamina III was virtually free from terminations, this layer does not appear to be of importance for the processing of primary afferent information from Group II/III receptors in deep tissues.