Multiphasic On/Off Pheromone Signalling in Moths as Neural Correlates of a Search Strategy

Abstract

Insects and robots searching for odour sources in turbulent plumes face the same problem: the random nature of mixing causes fluctuations and intermittency in perception. Pheromone-tracking male moths appear to deal with discontinuous flows of information by surging upwind, upon sensing a pheromone patch, and casting crosswind, upon losing the plume. Using a combination of neurophysiological recordings, computational modelling and experiments with a cyborg, we propose a neuronal mechanism that promotes a behavioural switch between surge and casting. We show how multiphasic On/Off pheromone-sensitive neurons may guide action selection based on signalling presence or loss of the pheromone. A Hodgkin-Huxley-type neuron model with a small-conductance calcium-activated potassium (SK) channel reproduces physiological On/Off responses. Using this model as a command neuron and the antennae of tethered moths as pheromone sensors, we demonstrate the efficiency of multiphasic patterning in driving a robotic searcher toward the source. Taken together, our results suggest that multiphasic On/Off responses may mediate olfactory navigation and that SK channels may account for these responses.

Reactive Searching and Infotaxis in Odor Source Localization

“…They are based on predefined movement sequences which are typically triggered by odor perceptions. Such biologically inspired strategies can be employed to locate pheromone sources [22] or other odors [23] – [26] , given appropriate sensors. In general, bio-inspired methods are widely discussed to overcome the challenges in chemical sensing [26] , [27] .…”

“…Using such an approach, we compare the strategies detailed above: reactive versus cognitive searching in dependence of the stimulation strength for a turbulent air flow. Our cyborg, a male moth Agrotis ipsilon mounted on a mobile robot [22] , has to find the pheromone source located two meters upwind from the starting position, see Fig. 1 .…”

“…The reactive strategies are derived from an analysis of electrophysiological recordings from the macroglomerular complex (MGC), the first cerebral relay for the processing of pheromone information perceived by olfactory receptor neurons (ORNs) in the moths' antennal lobe [9] , [38] . They show triphasic neuronal responses (On, inhibition, Off) to pheromone stimulation [22] , [39] . The origin of the inhibitory phase was the focus of [22] who employed reactive searching implemented on a cyborg in order to provide evidence that reactive searching could be mediated by multiphasic responses.…”

Using Insect Electroantennogram Sensors on Autonomous Robots for Olfactory Searches

“…Our EAG-robotic platform was primarily developed to test biological hypotheses about olfactory coding and search strategies in insects 13 . Similar to central neurons receiving input from insect antennae, we connected a neuron model to a real moth antenna on a robot and performed pheromone detection based on its firing pattern.…”

Olfactory coding in the turbulent realm

“…In our model, the inhibition phase was included in the shape of the linear filters, contributing to the difference between ORN and PN filters, in particular in the PC2 component. The inhibition phase results either from local inhibitory circuits [58][59][60] and/or from intrinsic PN properties [61]. It is noteworthy that inhibitory mechanisms have been hypothesized to enlarge the temporal bandwidth transmitted through ORN to PN synapses [62].…”