PHYSIOLOGICAL-PROPERTIES OF PRIMARY SENSORY NEURONS APPROPRIATELY AND INAPPROPRIATELY INNERVATING SKELETAL-MUSCLE IN ADULT-RATS

1. We have studied the physiology of primary sensory neurons innervating rat hindlimb muscle in the following: 1) normal control animals; 2) animals in which the gastrocnemius nerve (Gn) had regenerated to its original muscle target; and 3) animals in which the cutaneous sural nerve (Sn) had regenerated to a foreign target, muscle. 2. Single-unit recordings were made from 115 afferents in normal, intact animals. They had conduction velocities of 0.8-67.2 m/s, which were distributed with peaks at approximately 1.25, 17.5, and 47.5 m/s. Of the myelinated fibers, 88% had low-threshold mechanosensitive receptive fields and responded to ramp-and-hold stretches of the muscle. The large majority of these fibers (85%) gave slowly adapting responses to ramp-and-hold stretches or direct muscle probing. Stretch-sensitive afferents could be divided (on the basis of their responses to active muscle contraction) into in-parallel or in-series receptors (presumed muscle spindles and Golgi tendon organs, respectively). The in-parallel receptors out-numbered the in-series receptors by approximately 3:2. The 12% of fibers that were insensitive to stretches of the muscle in the physiological range could be divided into roughly equal groups of totally insensitive fibers and high-threshold fibers, which required excessive stretching of the muscle. 3. In the animals with regrown Gn, 94 single fibers with conduction velocities ranging from 11 to 60.6 m/s were studied. The myelinated conduction velocity distribution exhibited only one peak, at approximately 37.5 m/s. Only 67% of the afferents were stretch sensitive ( vs. 88% in normal animals), and only about two-thirds of these (vs. 85% in normal animals) gave slowly adapting responses to ramp-and-hold stretches or muscle probing. The incidence of in-series receptors was also increased among regenerated gastrocnemius afferents. The 33% of fibers that were stretch insensitive were mostly unresponsive to even extreme forms of mechanical stimuli. This group presumably represents afferents that failed to make appropriate endings. 4. In the animals with Sn directed to muscle, 460 single afferents were recorded. Their conduction velocities ranged from 0.7 to 67.9 m/s, and the distribution exhibited only a single peak for myelinated fibers at approximately 22.5 m/s, significantly lower than for intact or regrown Gn. Only 41% of the myelinated fibers were stretch sensitive. Nearly all of these (98%) were rapidly adapting to ramp-and-hold stretches or muscle probing, in marked contrast to the other groups. Also, unlike other groups, nearly all stretch-sensitive afferents appeared to be in-series. Of the 59% of afferents that were stretch insensitive, about one-half responded to gentle probing of the muscle, suggesting they were erstwhile low-threshold receptors that had failed to form suitable endings. 5. The results suggest that, when gastrocnemius afferents regenerate to muscle, some of their properties are altered. For instance, axonal conduction velocity decreases, fewer fibers form mechanosensitive endings, and those that do appear less mature. When the Sn reinnervates muscle, about two-thirds of the myelinated fibers form mechanosensitive endings in the foreign target. Thresholds are, on average, higher than normally found for muscle afferents, and only approximately 41% of fibers become responsive to muscle stretch. Nonetheless, some of the properties of sural afferents do appear to become more appropriate for the tissue that they newly innervate. For instance, axonal conduction velocity is higher for sural afferents regenerating to muscle than to skin.