Differential projections of B and C sympathetic axons in peripheral nerves of the bullfrog

Abstract

Accumulating evidence indicates that electrophysiologically distinct subsets of sympathetic neurons selectively innervate different classes of targets. The organization of this system may therefore be reflected in the sympathetic fiber contents of peripheral nerves. To test this possibility, we have mapped the pathways followed by three groups of postganglionic sympathetic axons in the bullfrog by recording compound action potentials and by retrograde tracing with horseradish peroxidase (HRP). The axons that were studied arise from fast B, slow B, and C-type neurons in ganglia 9 and 10 at the lumbar end of the paravertebral sympathetic chain. They project to peripheral targets primarily by way of the sciatic nerve and can be distinguished by the velocities with which they conduct action potentials. Action potentials were recorded with suction electrodes from isolated preparations composed of paravertebral chain ganglia 7-10, the sciatic nerve, and branches of the sciatic nerve that supply striated muscles, skin, and the bladder. Preganglionic B fibers were selectively activated by stimulating the paravertebral chain rostral to ganglion 7, and preganglionic C fibers were selectively activated by stimulating spinal nerves 7 and 8 at points central to their rami communicantes. Compound action potentials recorded from the sciatic, peroneal, tibial, and sural nerves and from the primary trunk of the pelvic nerve were each found to contain three components produced, respectively, by fast B, slow B, and C-type sympathetic axons. Similarly, action potentials recorded from cutaneous branches of the sciatic tree were found to contain three sympathetic components. By contrast, when compound action potentials were recorded from branches of the sciatic tree that directly enter and innervate striated muscles and also the bladder, the sympathetic responses were found to arise solely from C-type axons. HRP was used to label the sympathetic neurons that project to the sartorius muscle and into the cutaneous lateral crural nerve. Retrograde transport of HRP from the sartorius muscle labeled 17 +/- 4 (mean +/- s.d.) sympathetic neurons and 27 +/- 3 spinal motoneurons while transport from the lateral crural nerve labeled 68 +/- 47 sympathetic neurons but no spinal neurons. The average somatic diameter of ganglion cells projecting to the sartorius muscle was significantly smaller than that of cells projecting to the lateral crural nerve. The electrophysiological results indicate that fast B and slow B sympathetic axons in the sciatic trunk and its primary branches project selectively into cutaneous nerves while sympathetic C axons project into all peripheral nerves.(ABSTRACT TRUNCATED AT 400 WORDS)

In vitro relation between preganglionic sympathetic stimulation and activity of cutaneous glands in the bullfrog.

“…If one assumes that these events were triggered by spontaneous action potentials, then this suggests that the area of skin under study was innervated by a small number of axons. It is also consistent with previous results from retrograde labelling of the nearby cutaneous lateral crural nerve, which contains only about thirty-five postganglionic B axons (Horn et al 1988). If evoked responses in our preparations were mediated by one or two axons, then it should be possible to measure their contributions by varying the strength of stimuli applied to the preganglionic pathway.…”

“…In addition, the two cell types control different targets. C neurones selectively innervate arteries in muscles and skin, and B neurones selectively project to non-vascular cutaneous targets (Horn, Stofer & Fatherazi, 1987;Horn, Fatherazi & Stofer, 1988;Stofer, Fatherazi & Horn, 1990;Horn, 1992). The goal of the present experiments was to develop a preparation of ganglia and skin that could be used to identify a target of B neurones and the peripheral consequences of ganglionic cotransmission.…”

Role of ganglionic cotransmission in sympathetic control of the isolated bullfrog aorta.

“…A stiff stainless-steel wire (0f41 mm diameter) was then threaded through the lumen and secured to the chamber bottom with U-shaped minutien pins. Next, separate stimulating electrodes were fitted to the preganglionic B and C pathways, and recording electrodes were fitted to the sciatic nerve or a postganglionic ramus from ganglia 9 or 10 (Dodd & Horn, 1983a;Horn, Fatherazi & Stofer, 1988; Thorne et al 1995). After securing the electrodes, a second steel wire (0'35 mm) was threaded through the aorta.…”

In vivo activity of B‐ and C‐neurones in the paravertebral sympathetic ganglia of the bullfrog.

“…Peripheral targets for neurones in paravertebral sympathetic ganglia of the bullfrog (BFSG) include the bladder, mucous and granular glands, as well as blood vessels in the skin and in striated muscles. Stimulation of the preganglionic C-fibres causes vasoconstriction in the skin and muscle (Honma, 1970;Yoshimura, 1979;Horn, Fatherazi & Stofer, 1988;Stofer, Fatherazi & Horn, 1990), whereas stimulation of B-fibres produces secretion from cutaneous glands (Honma, 1970;Lang, Sjoberg & Skoglund, 1975), modulation of the sensitivity of cutaneous mechanoreceptors (Loewenstein, 1956) and a shortening of the recovery of arterioles which had been previously constricted following C-fibre stimulation (Yoshimura, 1979). The B-fibre and C-fibre systems originate from separate groups of neurones in the spinal cord and remain anatomically separate as they pass through the paravertebral ganglia (Nishi & Koketsu, 1960;Dodd & Horn 1983a;; but see also Smith & Weight, 1986).…”