Brief Exposure to Sensory Cues Elicits Stimulus- Nonspecific General Sensitization in an Insect Sebastian Minoli1,2., Isabella Kauer1,3., Violaine Colson1,4, Virginie Party1, Michel Renou 1 , Peter Anderson 5 , Christophe Gadenne1,6, Fre´ de´ ric Marion-Poll1,7, Sylvia Anton1,6* 1 INRA, UMR 1272 Physiologie de l’Insecte, Versailles, France, Universite´ Pierre et Marie Curie, Paris, France, 2 Departmento Biodiversidad y Biolog´ıa Experimental, FCEyN, Universidad de Buenos Aires, Ciudad Universitaria, Buenos Aires, Argentina, 3 Department of Systems and Computational Neurobiology, MPI of Neurobiology, Martinsried, Germany, 4 INRA, UR 1037 Laboratoire de Physiologie et Ge´nomique des Poissons, Campus de Beaulieu, Rennes, France, 5 Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Alnarp, Sweden, 6 Laboratoire Re´cepteurs et Canaux Ioniques Membranaires, Universite´ d’Angers, UPRES EA 2647 USC INRA 1330, Angers, France, 7 De´partement Sciences de la Vie et Sante´, AgroParisTech, Paris, France 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. Citation: Minoli S, Kauer I, Colson V, Party V, Renou M, et al. (2012) Brief Exposure to Sensory Cues Elicits Stimulus-Nonspecific General Sensitization in an Insect. PLoS ONE 7(3): e34141. doi:10.1371/journal.pone.0034141 Editor: Melissa J. Coleman, Claremont Colleges, United States of America Received December 15, 2011; Accepted February 22, 2012; Published March 23, 2012 Copyright: 2012 Minoli et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by French National Founding Agency Grant ANR-07-NEURO-037- 01 to SA, FMP and MR, the Swedish Research Council (VR), Trygger Foundation and a Linnaeus Grant from the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas) to PA. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: sylvia.anton@angers.inra.fr . These authors contributed equally to this work. Introduction Animals are innately sensitive to many biologically relevant cues of different sensory modalities originating from their environment. However, being able to adjust their innate behavioural responses according to their past experiences might be the key for adapting to a changing environment. Besides transitory and reversible effects on the sensory-motor systems that occur within a time frame of milliseconds to several minutes, experience can also have a profound effect on how sensory systems develop as demonstrated in vertebrates for the visual [1,2], auditory [3], somatosensory [2] and olfactory systems [4,5], both at the peripheral and central levels. In most cases, 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]. Experience can, however, induce a change of sensitivity in two directions. Habituation, defined as the decrease in a behavioural response after repeated presentations of the same stimulus [7] is an experience-mediated plasticity through which animals may learn to filter out external information that is not relevant any more [8,9]. 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 [10–13]. Both sensitization and habituation are forms of non-associative learning, lacking a reward or a punishment. Contrarily, associative learning entails assigning a meaning for a previously neutral stimulus after the simultaneous occurrence with a reinforcement [14,15]. Some of the underlying processes that provoke changes in sensitivity of the chemosensory system of insects have already been described [16–19]. Recently, we found that a brief exposure to sex pheromone could sensitize males of the noctuid moth Spodoptera littoralis to this pheromone long after the presentation of the stimulus. Males briefly exposed to the female pheromone gland extract or to the principal component of the female sex pheromone (Z,E-9,11- tetradecadienyl acetate, Z,E-9,11-14:OAc) were more sensitive to the same pheromone than naive males 27 h after the exposure [13,19]. This increase of behavioural sensitivity was correlated with an increased sensitivity of antennal lobe (AL) neurons to sex PLoS ONE | www.plosone.org 1 March 2012 | Volume 7 | Issue 3 | e34141