Brief Exposure to Sensory Cues Elicits Stimulus-Nonspecific General Sensitization in an Insect

Sebastian Minoli,Isabella Kauer,Christophe Gadenne,Virginie Party,Michel Renou,Sylvia Anton,Peter Anderson,Violaine Colson,Frédéric Marion-Poll,Melissa J. Coleman

doi:10.1371/journal.pone.0034141

Abstract

The effect of repeated exposure to sensory stimuli, with or without reward is well known to induce stimulus-specific modifications of behaviour, described as different forms of learning. In recent studies we showed that a brief single pre-exposure to the female-produced sex pheromone or even a predator sound can increase the behavioural and central nervous responses to this pheromone in males of the noctuid moth Spodoptera littoralis. To investigate if this increase in sensitivity might be restricted to the pheromone system or is a form of general sensitization, we studied here if a brief pre-exposure to stimuli of different modalities can reciprocally change behavioural and physiological responses to olfactory and gustatory stimuli. Olfactory and gustatory pre-exposure and subsequent behavioural tests were carried out to reveal possible intra- and cross-modal effects. Attraction to pheromone, monitored with a locomotion compensator, increased after exposure to olfactory and gustatory stimuli. Behavioural responses to sucrose, investigated using the proboscis extension reflex, increased equally after pre-exposure to olfactory and gustatory cues. Pheromone-specific neurons in the brain and antennal gustatory neurons did, however, not change their sensitivity after sucrose exposure. The observed intra- and reciprocal cross-modal effects of pre-exposure may represent a new form of stimulus-nonspecific general sensitization originating from modifications at higher sensory processing levels.

Highlights

Animals are innately sensitive to many biologically relevant cues of different sensory modalities originating from their environment
When tested on a locomotion compensator with a pheromone stimulus (PHE), both naıve and pre-exposed males responded to 0.1 or 0.25 female equivalents (FE) of PHE orienting towards the source (Figure 1, Rayleigh test p,0.05 in all cases)
Both activity and orientation levels increased with increasing PHE concentrations in control and preexposed males (Figure 2, positive dose-response curves) and significant differences between pre-exposed and control-exposed males were observed for all three doses of PHE (0.1, 0.25 and 0.5 FE): in all cases, responses of pre-exposed males were higher than in naıve males

Summary

Introduction

Animals are innately sensitive to many biologically relevant cues of different sensory modalities originating from their environment. Experience with a given sensory cue induces a long-lasting increase of responsiveness to the same stimulus, as shown e.g. in the model organism Aplysia [6]. In this marine slug, a repeatedly applied noxious stimulus elicits a facilitated siphon withdrawal reflex for up to three weeks [6]. The opposite effect is sensitization, in which individuals become more sensitive to a stimulus of particular interest once it is present, and increase in this way the probability of finding the stimulus source, or contrarily to avoid it in the case of a noxious stimulus [10,11,12,13] Both sensitization and habituation are forms of non-associative learning, lacking a reward or a punishment. Some of the underlying processes that provoke changes in sensitivity of the chemosensory system of insects have already been described [16,17,18,19]

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Conclusion