scholarly journals Non-synaptic interactions between olfactory receptor neurons, a possible key feature of odor processing in flies

2021 ◽  
Vol 17 (12) ◽  
pp. e1009583
Author(s):  
Mario Pannunzi ◽  
Thomas Nowotny

When flies explore their environment, they encounter odors in complex, highly intermittent plumes. To navigate a plume and, for example, find food, they must solve several challenges, including reliably identifying mixtures of odorants and their intensities, and discriminating odorant mixtures emanating from a single source from odorants emitted from separate sources and just mixing in the air. Lateral inhibition in the antennal lobe is commonly understood to help solving these challenges. With a computational model of the Drosophila olfactory system, we analyze the utility of an alternative mechanism for solving them: Non-synaptic (“ephaptic”) interactions (NSIs) between olfactory receptor neurons that are stereotypically co-housed in the same sensilla. We find that NSIs improve mixture ratio detection and plume structure sensing and do so more efficiently than the traditionally considered mechanism of lateral inhibition in the antennal lobe. The best performance is achieved when both mechanisms work in synergy. However, we also found that NSIs decrease the dynamic range of co-housed ORNs, especially when they have similar sensitivity to an odorant. These results shed light, from a functional perspective, on the role of NSIs, which are normally avoided between neurons, for instance by myelination.

2020 ◽  
Author(s):  
Mario Pannunzi ◽  
Thomas Nowotny

AbstractWhen flies explore their environment, they encounter odors in complex, highly intermittent plumes. To navigate a plume and, for example, find food, flies must solve several tasks, including reliably identifying mixtures of odorants and discriminating odorant mixtures emanating from a single source from odorants emitted from separate sources and mixing in the air. Lateral inhibition in the antennal lobe is commonly understood to help solving these two tasks. With a computational model of the Drosophila olfactory system, we analyze the utility of an alternative mechanism for solving them: Non-synaptic (“ephaptic”) interactions (NSIs) between olfactory receptor neurons that are stereotypically co-housed in the same sensilla. For both tasks, NSIs improve the insect olfactory system and outperform the standard lateral inhibition mechanism in the antennal lobe. These results shed light, from an evolutionary perspective, on the role of NSIs, which are normally avoided between neurons, for instance by myelination.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Gregor A. Bergmann ◽  
Gerd Bicker

AbstractLocusts are advantageous organisms to elucidate mechanisms of olfactory coding at the systems level. Sensory input is provided by the olfactory receptor neurons of the antenna, which send their axons into the antennal lobe. So far, cellular properties of neurons isolated from the circuitry of the olfactory system, such as transmitter-induced calcium responses, have not been studied. Biochemical and immunocytochemical investigations have provided evidence for acetylcholine as classical transmitter of olfactory receptor neurons. Here, we characterize cell cultured projection and local interneurons of the antennal lobe by cytosolic calcium imaging to cholinergic stimulation. We bulk loaded the indicator dye Cal-520 AM in dissociated culture and recorded calcium transients after applying cholinergic agonists and antagonists. The majority of projection and local neurons respond with increases in calcium levels to activation of both nicotinic and muscarinic receptors. In local interneurons, we reveal interactions lasting over minutes between intracellular signaling pathways, mediated by muscarinic and nicotinic receptor stimulation. The present investigation is pioneer in showing that Cal-520 AM readily loads Locusta migratoria neurons, making it a valuable tool for future research in locust neurophysiology, neuropharmacology, and neurodevelopment.


PLoS ONE ◽  
2021 ◽  
Vol 16 (5) ◽  
pp. e0249798
Author(s):  
Johannes Reisert ◽  
Glen J. Golden ◽  
Michele Dibattista ◽  
Alan Gelperin

Peripheral sensory cells and the central neuronal circuits that monitor environmental changes to drive behaviors should be adapted to match the behaviorally relevant kinetics of incoming stimuli, be it the detection of sound frequencies, the speed of moving objects or local temperature changes. Detection of odorants begins with the activation of olfactory receptor neurons in the nasal cavity following inhalation of air and airborne odorants carried therein. Thus, olfactory receptor neurons are stimulated in a rhythmic and repeated fashion that is determined by the breathing or sniffing frequency that can be controlled and altered by the animal. This raises the question of how the response kinetics of olfactory receptor neurons are matched to the imposed stimulation frequency and if, vice versa, the kinetics of olfactory receptor neuron responses determine the sniffing frequency. We addressed this question by using a mouse model that lacks the K+-dependent Na+/Ca2+ exchanger 4 (NCKX4), which results in markedly slowed response termination of olfactory receptor neuron responses and hence changes the temporal response kinetics of these neurons. We monitored sniffing behaviors of freely moving wildtype and NCKX4 knockout mice while they performed olfactory Go/NoGo discrimination tasks. Knockout mice performed with similar or, surprisingly, better accuracy compared to wildtype mice, but chose, depending on the task, different odorant sampling durations depending on the behavioral demands of the odorant identification task. Similarly, depending on the demands of the behavioral task, knockout mice displayed a lower basal breathing frequency prior to odorant sampling, a possible mechanism to increase the dynamic range for changes in sniffing frequency during odorant sampling. Overall, changes in sniffing behavior between wildtype and NCKX4 knockout mice were subtle, suggesting that, at least for the particular odorant-driven task we used, slowed response termination of the odorant-induced receptor neuron response either has a limited detrimental effect on odorant-driven behavior or mice are able to compensate via an as yet unknown mechanism.


2012 ◽  
Vol 520 (8) ◽  
pp. 1687-1701 ◽  
Author(s):  
Hidehiro Watanabe ◽  
S. Shuichi Haupt ◽  
Hiroshi Nishino ◽  
Michiko Nishikawa ◽  
Fumio Yokohari

2014 ◽  
Vol 9 (8) ◽  
pp. 1934578X1400900 ◽  
Author(s):  
Carmen Quero ◽  
Berta Vidal ◽  
Angel Guerrero

Increased behavioral sensitivity to the pheromone after brief exposure of the whole insect to the sex pheromone has been documented in antennal lobe neurons of Spodoptera littoralis. We investigated whether a brief stimulus of the major component of the pheromone on naïve antenna separated from the head increased the electroantennographic responses after successive stimulations at different times. The response increase was clear 30 min after the first stimulation, and this effect lasted at least 60 min, the average life time of the antenna. Our results suggest that the olfactory receptor neurons, and not only the neurons in the antennal lobe, may be involved in the increased antennal response after a single pheromone pulse.


2021 ◽  
Author(s):  
Florencia Scarano ◽  
Mukilan Deivarajan Suresh ◽  
Ettore Tiraboschi ◽  
Amélie Cabirol ◽  
Morgane Nouvian ◽  
...  

Geosmin is an odorant produced by bacteria in moist soil. It has been found to be extraordinarily relevant to some insects, but the reasons for this are not yet fully understood. Here we report the first tests of the effect of geosmin on honey bees. A stinging assay showed that the defensive behaviour elicited by the bee's alarm pheromone is strongly suppressed by geosmin. Surprisingly, the suppression is, however, only present at very low geosmin concentrations, and completely disappears at higher concentrations. We investigated the underlying mechanisms of the behavioural change at the level of the olfactory receptor neurons by means of electroantennography and at the level of the antennal lobe output via calcium imaging. Unusual effects were observed at both levels. The responses of the olfactory receptor neurons to mixtures of geosmin and the alarm pheromone component isoamyl acetate (IAA) were lower than to pure IAA, suggesting an interaction of both compounds at the olfactory receptor level. In the antennal lobe, the neuronal representation of geosmin showed a glomerular activation that decreased with increasing concentration, correlating well with the concentration dependence of the behaviour. Computational modelling of odour transduction and odour coding in the antennal lobe suggests that a broader than usual activation of different olfactory receptor types by geosmin in combination with lateral inhibition in the antennal lobe could lead to the observed non-monotonic increasing-decreasing responses to geosmin and thus underlie the specificity of the behavioural response to low geosmin concentrations.


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