The Journal of Neuroscience, August 30, 2006, 26(35):8900-8908; doi:10.1523/JNEUROSCI.2351-06.2006
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Development/Plasticity/Repair
Temporal Coding Mediates Discrimination of "Bitter" Taste Stimuli by an Insect
John I. Glendinning,
Adrienne Davis, and
Meelu Rai
Department of Biological Sciences, Barnard College, Columbia University, New York, New York 10027
Correspondence should be addressed to John I. Glendinning, Department of Biological Sciences, Barnard College, Columbia University, 3009 Broadway, New York, NY 10027. Email: jglendinning{at}barnard.edu
The mechanisms that mediate discriminative taste processing in insects are poorly understood. We asked whether temporal patterns of discharge from the peripheral taste system of an insect (Manduca sexta caterpillars; Sphingidae) contribute to the discrimination of three "bitter" taste stimuli: salicin, caffeine, and aristolochic acid. The gustatory response to these stimuli is mediated exclusively by three pairs of bitter-sensitive taste cell, which are located in the medial, lateral, and epipharyngeal sensilla. We tested for discrimination by habituating the caterpillars to salicin and then determining whether the habituation generalized to caffeine or aristolochic acid. We ran habituation-generalization tests in caterpillars with their full complement of taste sensilla (i.e., intact) and in caterpillars with ablated lateral sensilla (i.e., lat-ablated). The latter perturbation enabled us to examine discrimination in caterpillars with a modified peripheral taste profile. We found that the intact and lat-ablated caterpillars both generalized the salicin-habituation to caffeine but not aristolochic acid. Next, we determined whether this pattern of stimulus-generalization could be explained by salicin and aristolochic acid generating distinct ensemble, rate, temporal, or spatiotemporal codes. To this end, we recorded excitatory responses from the bitter-sensitive taste cells and then used these responses to formulate predictions about whether the salicin-habituation should generalize to caffeine or aristolochic acid, separately for each coding framework. We found that the pattern of stimulus generalization in both intact and lat-ablated caterpillars could only be predicted by temporal coding. We conclude that temporal codes from the periphery can mediate discriminative taste processing.
Key words: taste; bitter; temporal coding; discrimination; insect; Manduca sexta
Received March 9, 2006;
revised July 17, 2006;
accepted July 24, 2006.
Correspondence should be addressed to John I. Glendinning, Department of Biological Sciences, Barnard College, Columbia University, 3009 Broadway, New York, NY 10027. Email: jglendinning{at}barnard.edu
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J. I. Glendinning, A. Jerud, and A. T. Reinherz
The hungry caterpillar: an analysis of how carbohydrates stimulate feeding in Manduca sexta
J. Exp. Biol.,
September 1, 2007;
210(17):
3054 - 3067.
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