Coding of odour and space in the hemimetabolous insect Periplaneta americana

Abstract

The 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 airspace 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 selectively labelling antennal lobe projection neurons with a calciumsensitive 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 a subregion 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.

Task-specific roles of local interneurons for inter -and intraglomerular signaling in the insect antennal lobe

“…The recordings were performed in the AL of the cockroach Periplaneta americana . This is an experimental system in which the olfactory system’s circuitry has been analyzed in great detail on the physiological (Bradler C, 2016; Ernst and Boeckh, 1983; Husch et al, 2009a, 2009b; Lemon and Getz, 1997, 1998, 2000; Nishino et al, 2012, 2018; Paeger et al, 2017; Paoli et al, 2020; Pippow et al, 2009; Strausfeld and Li, 1999; Warren and Kloppenburg, 2014; Watanabe et al, 2017), biochemical (Distler, 1989, 1990; Fusca et al, 2013, 2015; Neupert et al, 2012, 2018), and structural/ ultrastructural levels (Distler and Boeckh, 1997a, 1997b; Distler et al, 1998; Malun, 1991a, 1991b; Malun et al, 1993; Nishino et al, 2015; Watanabe et al, 2010), thus contributing very successfully to understanding olfactory information processing principles.…”

Odor processing in the cockroach antennal lobe—the network components

“…In turn, these OSNs form new layers of OSN terminals in the AL glomeruli from the core to the cortex. This age-specific and thus, segment-specific layer formation ultimately produces an antennotopic innervation of the glomeruli (Nishino et al 2018 ; Paoli et al 2020 ). The physiological relevance for spatial coding was confirmed for the macroglomerulus (MG) electrophysiologically (Hösl 1990 ; Nishino et al 2018 ) and most recently by Ca 2+ imaging (Paoli et al 2020 ).…”

“…The somata of these uPNs are located within the cluster of type 2 uPNs, and they also project to the mushroom body calyces and the LH via the mALT. In contrast to ordinary glomeruli, which normally contain the neurites of only one uPN, the MG is innervated by multiple uPNs with spatially distinct receptive fields on the antenna (Hösl 1990 ; Nishino et al 2018 ; Watanabe et al 2018 ; Paoli et al 2020 ). One PN, named “large receptive field” PN (L-PN) receives input from pheromone sensitive OSNs along the entire antennal flagellum and is hologlomerular.…”

“…Due to a lack of systematic electrophysiological studies (but see Strausfeld and Li (1999a, b), the function of these neurons remains enigmatic. As mPNs typically have neurites only in subglomerular portions and each glomerulus is covered by multiple mPNs, it is tempting to speculate that these neurons play a role in encoding spatial information similar to the S-PNs of the MG as discussed by (Galizia 2018;Paoli et al 2020).…”

Social modulation of individual preferences in cockroaches

“…We discover that the presence of a social odor influences individual shelter selection and monitor how food-and social-related olfactory information shape individual preference. To test how behavioral choices relate to the neural representation of the stimuli, we adopted a recently established method for selectively labeling the uniglomerular PNs population with a calcium sensitive dye for AL functional imaging (Paoli et al, 2020). Thus, combining neuroimaging with behavioral assays, we studied how food and colony odor cues, alone or combined, are encoded by the cockroach brain and how their perception guides behavioral choices.…”