Coding of odour and space in the hemimetabolous insect Periplaneta americana

Abstract

statementBy selective labelling the cockroach's antennal lobe output neurons, we investigated the logic of olfactory coding in a hemimetabolous insect, showing that odour responses are stimulus-specific, concentration-dependent, and preserve information on the spatial structure of the stimulus. AbstractThe general architecture of the olfactory system is highly conserved from insects to humans, but neuroanatomical and physiological differences can be observed across species. The American cockroach, inhabiting dark shelters with a rather stable olfactory landscape, is equipped with long antennae used for sampling the surrounding air-space for orientation and navigation. The antennae's exceptional length provides a wide spatial working range for odour detection; however, it is still largely unknown whether and how this is also used for mapping the structure of the olfactory environment. By selective labelling antennal lobe projection neurons with a calcium sensitive dye, we investigated the logic of olfactory coding in this hemimetabolous insect. We show that odour responses are stimulus-specific and concentration-dependent, and that structurally related odorants evoke physiologically similar responses. By using spatially confined stimuli, we show that proximal stimulations induce stronger and faster responses than distal ones. Spatially confined stimuli of the female pheromone periplanone-B activate sub-region of the male macroglomerulus. Thus, we report that the combinatorial logic of odour coding deduced from holometabolous insects applies also to this hemimetabolous species. Furthermore, a fast decrease in sensitivity along the antenna, not supported by a proportionate decrease in sensillar density, suggests a neural architecture that strongly emphasizes neuronal inputs from the proximal portion of the antenna. 1983; Schaller, 1978; Watanabe et al., 2012). Their axons innervate two exceptionally large glomeruli, which form the macroglomerular complex (Schaller, 1978; Watanabe et al., 2012).Glomeruli are interconnected by a dense network of local interneurons (Fusca et al., 2013; Husch et al., 2009), and processed olfactory information is relayed to higher order brain centres by uniglomerular (uPNs) and multiglomerular projection neurons (mPNs) (Malun et al., 1993).Uniglomerular PNs extend their dendritic arborization in a single glomerulus, thus receiving direct input from only one OSN type. Two subgroups of uPNs innervate distinct glomerular populations, their cell bodies clustering in two distinct groups in the antero-dorsal side of the AL (Strausfeld and Li, 1999; Watanabe et al., 2017). In the American cockroach, each ordinary glomerulus is innervated by only one uPN, whereas the macroglomerulus (MG) is innervated by multiple uPNs with a highly stereotyped topology (Galizia, 2018; Nishino et al., 2018). Two main PN axon bundles exit from the medio-dorsal side of the antennal lobe (note that all orientations here provided are in body axis system), and relay odour-related information to the protocerebrum. ...