A peripheral mechanism for behavioral adaptation to specific "bitter" taste stimuli in an insect

Animals have evolved several chemosensory systems for detecting potentially dangerous foods in the environment. Activation of specific sensory cells within these chemosensory systems usually elicits an aversive behavioral response, leading to avoidance of the noxious foods. Although this aversive behavioral response can be adaptive, there are many instances in which it generates "false alarms," causing animals to reject harmless foods. To minimize the number of false alarms, animals have evolved a variety of physiological mechanisms for selectively adapting their aversive behavioral response to harmless noxious compounds. We examined the mechanisms underlying exposure-induced adaptation to specific "bitter" compounds in Manduca sexta caterpillars. M. sexta exhibits an aversive behavioral response to many plant-derived compounds that taste bitter to humans, including caffeine and aristolochic acid. This aversive behavioral response is mediated by three pairs of bitter-sensitive taste cells: one responds vigorously to aristolochic acid alone, and the other two respond vigorously to both caffeine and aristolochic acid. We found that 24 hr of exposure to a caffeinated diet desensitized all of the caffeine-responsive taste cells to caffeine but not to aristolochic acid. In addition, we found that dietary exposure to caffeine adapted the aversive behavioral response of the caterpillar to caffeine, but not to aristolochic acid. We propose that the adapted aversive response to caffeine was mediated directly by the desensitized taste cells and that the adapted aversive response did not generalize to aristolochic acid because the signaling pathway for this compound was insulated from that for caffeine.