Quality coding of a complex odorant in an invertebrate

Abstract

Mechanisms whereby the olfactory system of the spiny lobster codes food odors were quantitatively analyzed. A 23-component chemical mixture, with a composition based on a tissue extract from a known food of lobsters, and 8 of the mixture's components were used to describe responses of single cells at two neural levels: a) olfactory receptor cells and b) low-order interneurons projecting from the main olfactory center of the brain. Cluster analysis identified six classes of narrowly tuned receptor cells. Interneurons, on the other hand, were significantly more broadly tuned than receptor cells and could not be grouped into a small number of discrete, highly correlated cell types. Nonetheless, some chemosensory interneurons (unimodal interneurons) had specificities as narrow as receptor cells. Across-neuron correlations between stimuli showed that the increase in neuronal breadth of responsiveness from the level of receptors to the level of interneurons was paralleled by an increase in similarity in across-neuron patterns and, therefore, a decline in ability to discriminate between any two compounds. Across-neuron correlations between concentrations of a given compound showed that stimulus quality had a much stronger effect on across-neuron patterns than did stimulus quantity and, hence, stimulus qualities could be distinguished in spite of concurrent changes in stimulus quantity. Coding of odor quality could be accomplished at the receptor level by a labeled-lines code. At the interneuronal level, odor quality appears to be coded by across-fiber patterns. However, the finding that unimodal interneurons were as narrowly tuned as receptor cells indicates that specific channels for some food-odor components (e.g., taurine and glycine) are conserved even at higher neuronal levels. These narrow-spectrum interneurons may have a special function in quality coding either by dominating the interneuronal across-fiber pattern for that stimulus or by being processed independently of the broad-spectrum interneurons and thereby transferring information about certain components by way of specific channels to even higher neuronal levels.