Neuronal processing of chemical information in crustaceans

Abstract

Most crustaceans live in aquatic environments and chemoreception is their dominant sensory modality. Crustacean chemoreception is mediated by small cuticular sense organs (sensilla) occurring on all body parts, with the antennules (first antennae), second antennae, legs, and mouthparts representing the major chemosensory organs. Chemoreceptive sensilla of crustaceans are divided into bimodal sensilla which comprise a few mechano- and some chemoreceptor neurons and occur on all appendages and aesthetascs which are innervated by 40-500 olfactory receptor neurons and exclusively occur on the antennular outer flagellum. Olfactory receptor neurons differ from chemoreceptor neurons of bimodal sensilla in having spontaneous activity, inhibitory responses, and autonomous bursting, but both types of receptor neurons mainly respond to small water-soluble molecules such as amino acids. The dichotomy in sensilla structure is reflected in the organization of the associated CNS pathways. Olfactory receptor neurons selectively innervate a synaptic region in the midbrain, the olfactory lobe, which is organized into dense substructures called glomeruli. As is typical of the first synaptic relay in the central olfactory pathway across metazoans, olfactory information processing in glomeruli is based on multiple types of inhibitory local interneurons and on projection neurons ascending to higher brain areas. Receptor neurons from bimodal sensilla target synaptic areas that are distributed throughout the brain and ventral nerve cord and contain arborizations of motoneurons innervating muscles of the segmental appendages that provide the chemo- and mechanosensory input. Based on the matching dichotomy of sensilla construction and of sensory pathway organization, we propose that crustacean chemoreception is differentiated into two fundamentally different modes: "olfaction" - chemoreception mediated by the aesthetasc-olfactory lobe pathway, and "distributed chemoreception" - chemoreception mediated by bimodal sensilla on all appendages and the associated synaptic areas serving as local motor centers. In decapod crustaceans, pheromone detection and processing of pheromone information are not mediated by dedicated sensilla and CNS pathways, respectively, but seem to be integral components of olfaction and distributed chemoreception. Aesthetascs mediate responses to distant pheromones, whereas bimodal sensilla located on the appendages touching the conspecific partner are likely responsible for the detection of contact pheromones.