The Journal of Neuroscience, May 15, 2001, 21(10):3688-3696
A Peripheral Mechanism for Behavioral Adaptation to Specific
"Bitter" Taste Stimuli in an Insect
John I.
Glendinning,
Hannah
Brown,
Maya
Capoor,
Adrienne
Davis,
Amakoe
Gbedemah, and
Eliza
Long
Department of Biological Science, Barnard College, Columbia
University, New York, New York 10027
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.
Key words:
taste cell; plasticity; long-term adaptation; bitter
taste; ingestive behavior; Manduca sexta
Copyright © 2001 Society for Neuroscience 0270-6474/01/21103688-09$05.00/0