Olfactory development in invertebrates. On the scent of central developmental issues

Invertebrate olfactory systems offer many advantages for cellular and molecular studies of development and for functional studies of developmental plasticity. For example, nematodes have chemical senses that can be studied using genetic approaches. Arthropods, which include insects and crustacea, have the advantages that certain neurons can be reliably identified from one individual to another, and that olfactory receptor neurons are located on peripheral appendages and thus can be manipulated independently of their brain targets even very early in development. Among the insects, olfactory learning can be displayed and used as a basis for studying olfactory plasticity in bees; genes are especially tractable in flies; individual growth cones can be visualized in the grasshopper embryo; and receptor neurons and glomeruli of known olfactory specificity and behavioral significance can be followed during early development in moths. In addition, many insect nervous systems are amenable to organ culture and dissociated-cell culture, opening the door to experimental studies of cellular interactions that can not be performed in situ. Recent research in the moth Manduca sexta attempts to identify the nature of the interactions between olfactory sensory axons, olfactory neurons of the brain, and glial cells in the creation of the array of glomeruli that underlie olfaction in the adult. Results indicate that timing of the ingrowth of olfactory receptor axons is critical for normal glomerulus development, that a subset of axons expresses a fasciclin II-like molecule that may play a role in guidance of their growth, and that glial cells must surround developing glomeruli in order to stabilize the 'protoglomerular' template made by receptor axon terminals. Moreover, glial cells are dye-coupled to each other early in glomerulus development and gradually become uncoupled. Electrical activity in neurons is not necessary for glomerulus formation; and some intercellular interactions, perhaps involving soluble factors, appear to involve tyrosine phosphorylation. In sum, a detailed picture is emerging of the cellular interactions that lead to the formation of glomeruli.