Temporal Coding Mediates Discrimination of “Bitter” Taste Stimuli by an Insect

Abstract

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 latablated caterpillars could only be predicted by temporal coding. We conclude that temporal codes from the periphery can mediate discriminative taste processing.

Pharmacological analysis of the feeding response of codling moth (Cydia pomonella; Lepidoptera: Tortricidae) neonates to bitter compounds

“…In caterpillars of Manduca sexta, these cells respond to substances that are perceived as bitter by humans: aristolochic acid, caffeine and salicin (Glendinning et al, 2006) and as a consequence, caterpillars reduce their feeding activity (Glendinning et al, 1999). Similar results are reported for caterpillars of Helicoverpa armigera and Bombyx mori (Zhang et al, 2013).…”

Not all sugars are created equal: some mask aversive tastes better than others in an herbivorous insect

“…We used (1) 200mmoll -1 Suc and Glu because it is the lowest concentration of each sugar that elicits a maximal excitatory response in both the lateral and medial styloconic sensilla; (2) 1mmoll -1 Ino because it elicits response similar in magnitude to 200mmoll -1 Suc in the lateral styloconic sensillum; and (3) 0.1mmoll -1 AA (sodium salt) and 5mmoll -1 Caf because they elicit robust aversive responses in M. sexta (Glendinning et al, 2006). We purchased all chemicals from Sigma-Aldrich (St Louis, MO, USA).…”

The hungry caterpillar: an analysis of how carbohydrates stimulate feeding inManduca sexta

“…Insects use several coding mechanisms to identify and discriminate taste stimuli, including labeled-line (Marella et al, 2006), temporal (Glendinning et al, 2006) and ensemble (Dethier and Crnjar, 1982;Glendinning et al, 2002) ), the spikes were limited to two classes of carbohydrate-sensitive taste cell and the caterpillars failed to exhibit significant feeding stimulation (Table·1, Fig.·9). However, the mixture of sucrose+inositol elicited a comparable peripheral response (i.e.…”

“…Despite displaying a robust aversive response to bitter stimuli (Frazier, 1986;Glendinning et al, 1999;Glendinning et al, 2006), M. sexta shows a weak-to-nonexistent appetitive response to amino acids and carbohydrates (Bowdan, 1995;Glendinning et al, 2000). The lackluster appetitive response to carbohydrates is perplexing because the peripheral gustatory system of M. sexta responds vigorously to carbohydrates.…”