Antennular grooming behavior (AGB) is a stereotyped behavior in crustaceans in which the first pair of antennae, the major olfactory organs, are clasped and wiped repetitively by the third maxillipeds, which also serve as feeding appendages. AGB apparently functions to clear away accumulating debris on or between the antennular aesthetascs (olfactory sensilla). The purpose of this research was to determine whether AGB can be activated by chemicals commonly found in food odors. Lobsters were presented, via headset or handheld pipette, with 27 chemicals found in their food. One chemical, L-glutamate, evoked very high frequencies of wiping. Most chemicals tested were not stimulatory and only a few were weakly stimulatory (adenosine-5'-monophosphate, glycine, D-glutamate). This is surprising because previous studies have shown that other behaviors (antennular flick, search) can be evoked by a much broader array of chemicals found in food odorants. On the basis of these results, we propose that chemosensory neurons that specifically detect L-Glu activate AGB through a recently described non-olfactory pathway. Furthermore, we propose that the role of L-Glu in evoking AGB is based on its electrostatic properties. Because it has a high probability of electrostatic adherence to the antennular cuticle, L-Glu is a sensitive indicator of fouling by food-associated chemicals and thus an appropriate compound to stimulate antennular grooming.
1. Neural coding of chemical mixtures was studied with the use of the peripheral olfactory system of the spiny lobster. The occurrence of mixture interactions (i.e., where the observed response to a mixture deviates significantly from the expected response) in individual cells and the effect of such mixture interactions on the coding of odorant intensity by populations of cells were examined. 2. Extracellular recordings of spiking activity of 98 primary olfactory receptor cells in the antennules were measured in response to seven compounds [adenosine-5'-monophosphate (AMP), betaine (Bet), L-cysteine (Cys), L-glutamate (Glu), ammonium chloride (NH4), DL-succinate (Suc), and taurine (Tau)] and their binary mixtures. To identify mixture interactions, observed responses to a range of concentrations of a binary mixture were compared with the predicted responses based on three mathematical models: a single receptor model, which assumes that the two compounds of a mixture bind to the same receptor site; a multiple receptor model, which assumes that the two compounds bind to two independent receptor sites; and a mixed composition receptor model, which incorporates our current state of knowledge of transduction processes in olfactory receptor cells of spiny lobsters. 3. Mixture interactions in individual cells were common: statistically significant mixture interactions were observed in 25% of the possible cases (Fig. 5). Suppression was much more common than enhancement. 4. Mixture interactions had significant effects on the absolute response magnitudes for a population of cells, which could be used as the neural code for stimulus intensity in this system. These effects are called intensity mixture interactions (Figs. 6-11). Intensity mixture interactions occurred for approximately 50% of the binary mixtures and were almost exclusively suppression (Figs. 12 and 13). The intensity mixture interactions were concentration independent. 5. The results suggest that mixture interactions in individual olfactory cells can result in intensity mixture interactions in the neuronal population such that there is a decrease in sensitivity to binary mixtures relative to what is expected based on the responses to individual components of the mixtures.
Crustaceans such as crabs and lobsters clean or 'groom' their olfactory organ, the antennule, by wiping it through a pair of mouthpart appendages, the third maxillipeds. In the lobster, only a few chemicals found in prey extracts, especially glutamate, elicit grooming. Chemosensory input driving grooming is likely to be mediated via sensilla located on antennules and third maxillipeds. Chemosensory antennular sensilla are innervated by neurons with central projections either to the glomerular olfactory lobe (aesthetasc sensilla) or to non-glomerular antennular neuropils (nonaesthetasc sensilla). By selectively ablating the chemosensory sensilla on the antennules and the third maxillipeds we have determined that the aesthetascs are necessary and sufficient to drive grooming behavior. Chemosensory activation of antennular grooming behavior likely follows a 'labeled-line' model in that aesthetasc neurons tuned to glutamate provide adequate input via the olfactory lobe to motor centers in the brain controlling antennular movements.
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