Gustatory trophic action of arterial chemosensory neurones in the cat.

The proximal stump of the carotid sinus nerve (c.s.n.) branch of the IXth cranial nerve was surgically cross-anastomosed to the distal stump of the lingual nerve (l.n.) branch of the same cranial nerve to test the ability of regenerating c.s.n. axons to reinnervate and induce taste buds on cat circumvallate papillae. The l.n. branch of the IXth nerve, which normally innervates circumvallate papillae, was directed away from the tongue by suturing it to the distal stump of the c.s.n. Animals with normal and re-anastomosed (cut, then resutured) l.n. served as control preparations. 2-19 months following cross-anastomosis, circumvallate papillae contained 59.8 +/- 9.1% (mean +/- S.E. of mean) of the normal incidence of taste buds, indicating that axons possessing specific gustatory trophic properties had reinnervated the epithelium. Further experimentation was concerned with confirming the identity of the putative foreign axons which reinnervated the taste buds. Radiolabelled axoplasmic transport and autoradiography showed that 89 +/- 4.4% of the taste buds in cross-anastomosed, and 97 +/- 2.1% in normal preparations were innervated by axons from the principal sensory ganglion (petrosal) of the IXth nerve (P greater than 0.05). Whole-nerve recordings in cross-anastomosed preparations demonstrated gustatory activity in the transposed c.s.n., which was similar to responses present in normal and re-anastomosed l.n. preparations. The largest response was evoked by 4 M-NaCl, followed by 1 M-NH4Cl and 0.02 M-quinine HCl. Sucrose (0.5 M) elicited insignificant nerve activity. In normal animals, gustatory or mechanical stimulation did not alter cardiopulmonary function, but in bilaterally cross-anastomosed preparations, gustatory stimuli produced respiratory excitation while mechanical stimulation resulted in reductions in blood pressure and respiratory inhibition. These data suggest that following cross-anastomosis, arterial chemosensory axons innervate taste buds and barosensory axons innervate tongue mechanoreceptors (which normally evoke cardiopulmonary reflexes from the carotid body and carotid sinus, respectively). We conclude that arterial chemosensory neurones share with gustatory chemosensory neurones a trophic function essential for the development and maintenance of taste buds.