The generalization of an olfactory-based conditioned response reveals unique but overlapping odour representations in the moth Manduca sexta.

Abstract

Most highly derived olfactory systems, such as the insect antennal lobe, discriminate among a wide array of monomolecular odourants and blends of odourants. Given the relatively limited number of neurons used to code these odours, this ability implies that neural representations for odours overlap in a cross-fiber coding scheme. Here we use the generalization of a conditioned feeding response in the sphinx moth, Manduca sexta, to quantify three geometry-based dimensions of odour space in which monomolecular odours may be assessed. In a series of experiments we show that generalization of a conditioned response from one monomolecular odour to another is a function of differences in length and shape of the carbon chain as well as the functional group on the molecule. When moths were conditioned to 2-hexanone or 1-decanol and tested with a number of alcohols and ketones, we found that the generalization of the conditioned response decreased as a function of the chain length and functional group. In contrast, when conditioned to 1-hexanol, moths failed to distinguish alcohols from ketones of the same chain length. In all of these cases, chain length did not interact with functional group, thus indicating the independence of these dimensions. Differential conditioning of alcohols and of alcohols and ketones revealed interaction of excitatory and inhibitory generalization gradients within an odour 'dimension'. When odourants were sufficiently distinct, the peak of the generalization gradient was shifted away from the conditioning odour and in an opposite direction from the unreinforced odour. Altogether, these data substantiate the claim that these molecular characteristics are relevant coding dimensions in the moth olfactory system. These data are consistent with a cross-fiber coding scheme in which odours are coded by spatio-temporally overlapping sets of neurons, both in the periphery and in the antennal lobes.