Catecholaminergic (CA) phenotypic characteristics have recently been detected in adult sensory neurons, demonstrating that CA expression in the periphery extends beyond the sympathoadrenal axis. Consequently, we may now determine whether common principles underlie CA phenotypic organization in functionally and embryologically diverse populations of peripheral neurons. To begin defining sensory transmitter regulation, the present study examined the relationship of CA expression to sensory target innervation in cranial nerve ganglion cells of the adult rat. Retrograde labeling combined with tyrosine hydroxylase (TH) immunocytochemistry indicated that 80-90% of CA sensory neurons in the glossopharyngeal petrosal ganglion project peripherally in the carotid sinus nerve (CSN). Most of these cells innervate a single target, the carotid body, revealing a striking correlation between CA expression and the pattern of sensory target innervation. Furthermore, CSN transection resulted in a transient marked decrease in TH catalytic activity and immunoreactivity within 1 week. Activities returned to normal by 3 weeks. Thus, axotomy reversibly decreased sensory TH, reproducing effects observed with central CA neurons (Ross et al., 1975), but differing in certain aspects from observations with sympathetic CA neurons (Cheah and Geffen, 1973; Kessler and Black, 1979). To determine whether disruption of axonal transport itself decreased TH in petrosal neurons, colchicine cuffs were placed around the intact CSN. Colchicine blockade reproduced the effects of axotomy, suggesting that deranged transport, and not axonal damage per se, altered TH. Finally, we studied the role of sensory projections to the CNS by examining petrosal TH after glossopharyngeal nerve rhizotomy. In contrast to sequelae of peripheral axotomy, rhizotomy did not alter TH, suggesting that projections to the periphery predominate in regulation of sensory TH.(ABSTRACT TRUNCATED AT 250 WORDS)