Olfactory excitation of interneurons in the brain of the spiny lobster

Summary

Multimodal interneurons descending the circumesophageal connectives from the brain to the lower nervous system in decapod crustaceans respond to stimulation of cephalic sensory structures. Using intracellular recording and staining and backfilling techniques, we have examined the complexity of olfactory stimulants necessary to excite descending interneurons in the spiny lobster, and have characterized the dendritic branching pattern and responsiveness to multimodal stimulation of some of these neurons.

The excitation of descending interneurons by different chemical stimulants or by different concentrations of any one stimulant appears to vary only in intensity, not in temporal pattern (Figs. 1, 2). Responses to chemical stimulation of chemoexcited interneurons at this level in the olfactory pathway resemble responses of primary receptors.

Variation in the responses of chemoexcited interneurons is attributable to differences between chemical stimulants (Table 2). Two mixtures of amino acids plus betaine at concentrations proportional to their occurrence in potential foods (‘crab’ and ‘urchin’; Table 1) are more excitatory than a mixture of inverted composition or a single component, glutamic acid. Another single component, taurine, is as excitatory as equimolar ‘crab’ and ‘urchin’ mixtures.

Individual chemoexcited interneurons exhibit different response spectra (Fig. 1; Tables 3, 4). Most are excited by taurine, for which there are specific antennular receptors, as well as by glutamic acid or betaine, indicating that convergence of odor qualities occurs within the olfactory pathway. Many interneurons exhibit similar concentration-response functions for taurine (Fig. 3) regardless of their responsiveness to other chemical stimulants (Table 3) or modalities (Table 4).

Many chemoexcited interneurons receive bilateral chemical, tactile and visual inputs. Spatial convergence of olfactory inputs is indicated by responses of many cells to stimulation of both the ipsilateral and contralateral antennules. A few cells respond only to ipsilateral chemical stimulation.

The morphological diversity of descending interneurons excited by stimulation of cephalic structures is evidenced by the variety of their dendritic branching patterns (Figs. 4–6). One striking characteristic of many chemoexcitated interneurons is the presence of extensive branching in the ipsilateral antennary neuropil (Fig. 6). Chemoexcited interneurons do not appear to contact the olfactory lobes, where the majority of the primary afferents terminate, and thus they presumably transmit at least third-order chemosensory information.

Because it is unlikely that chemosensory information is further processed per se in the subesophageal nervous system, our results suggest that the chemosensory output of the spiny lobster brain is encoded by a heterogeneous population of interneurons.