Capacity of Visual Classical Conditioning in Drosophila Larvae

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Capacity of Visual Classical Conditioning in Drosophila Larvae Capacity of Visual Classical Conditioning in Drosophila Larvae Alina M. H. J. von Essen Dennis Pauls University of Fribourg Philipps-University Marburg Andreas S. Thurn and Simon G. Sprecher University of Fribourg Vision is an ancient sense essential for various aspects of animal behavior. Visual information not only leads to immediate, temporary, and rapid behavioral responses but also has lasting effects. NaIve behavioral responses to light are not always identical but can be altered based on positive or negative experience-a process defined as visual learning. In this study, Drosophila larvae were used as a simple model to study visual classical conditioning. We show that larvae are able to associate positive or negative cues with either light or darkness, thus changing their native light-preference. This effect can be robustly provoked through gustatory stimuli and electric shock. We further show that light can not only be used as a conditioned stimulus but also as an unconditioned stimulus, as punishment in the olfactory classical conditioning procedure, possibly forming two different kinds of memories. Our findings show that even though larvae show a strong naiVe response when exposed to light, the animals display a comparably large repertoire of visual memories that can be formed. Therefore, our study provides an impacting entry point into the genetic dissection of the neuronal circuit that underlies different types of visual learning. KeYlVords: Drosophila, visual learning, classical conditioning, larval behavior Learning and memory affect fundamental aspects of everyday (Nassif, Noveen, & Hartenstein, 2003). The brain of the Drosoph­ life. Defects in these brain functions are correlated with serious ila larva is at least one order of magnitude simpler in complexity human neurodegenerative conditions such as Alzheimer's disease in terms of neuron number and connectivity than its adult coun­ (Hirth, 2010; Xia, 2010; Ashe & Zahs, 2010). Therefore, resolving terpart. In striking contrast to its simplicity, it displays a wide the anatomical and molecular basis of higher brain functions range of a behavioral repertoire, which makes the Drosophila larva remains a scientific goal of wide interest. Toward this aim, differ­ an excellent model system to study different aspects of learning ent animal models have been used to study learning and memory, and memory (Gerber & Stocker, 2007). including the fruit fly, Drosophila melanogaster (Heisenberg, Two important functions rely on the larval eye, also termed 2003; Keene & Waddell, 2007; Fiala, 2007). Drosophila shares Bolwig's organ (BO). When exposed to light, Drosophila larvae many organizational features with the mammalian central nervous display striking negative phototaxis (Sawin-McCormack, system. However, the adult Drosophila brain consists of up to Sokolowski, & Campos, 1995). Another capacity of the visual 10,000 times less neurons compared with the mammalian brain system is the light-dependent entrainment of the molecular clock to control the circadian rhythm, which results in alternating de­ grees of photonegative behavior over the course of the day (Maz­ zoni, Desplan, & Blau, 2005). In contrast to these well-established fields, only little is known in regard to the capacity on larval visual Alina M. H. J. von Essen, Andreas S. Thum, and Simon G. Sprecher, associative learning (Gerber et aI., 2004; Knight, Iliadi, Charlton, Department of Biology, Institute of Cell and Developmental Biology, University of Fribourg, Fribourg, Switzerland; Dennis Pauls, Department Atwood, & Boulianne, 2007). of Biology, Institute of Neurobiology/Ethology, Philipps-University Mar­ Learning and memory in Drosophila larvae has been studied burg, Marburg, Germany. mainly for classical olfactory conditioning. Thereby, animals can Andreas S. Thum is now at the Department of Biology, University of learn to avoid an odor (the conditioned stimulus [CS]) that was Konstanz, Konstanz, Germany. paired with an aversive unconditioned stimulus (US; e.g., high salt We thank our colleagues of the Thum lab, Stocker lab, and Sprecher lab concentrations, quinine, or electric shock). Conversely, if the same for fruitful discussions and helpful comments on the manuscript. This work odor (CS) is paired with an appetitive US (e.g., sugar), animals was financially supported by the Swiss National Science Foundation develop a preference for it (Gerber & Stocker, 2007; Pauls, Pfit­ (PPOOP3_ 123339 to S. G. S. and 31003A_132812 to A. S. T.). Correspondence concerning this article should be addressed to Simon G. zenmaier, et aI., 2010). Thus, depending on previous experience, Sprecher, Department of Biology, Institute of Cell and Developmental the same odor can trigger either avoidance or attraction (Gerber & Biology, University of Fribourg, Ch. du Musee 10, CH 1700 Fribourg, Hendel, 2006). In contrast, vi sual learning in Drosophila larvae Switzerland. E-mail: [email protected] was only demonstrated when light or darkness was paired with 921 922 positive sugar reinforcement using individual larvae. Using the over 5 min compared to half-illuminated agarose plates (data not same protocol, negative reinforcement (salt and quinine) did not shown). Therefore, we used quadrant pl ates for all our learning lead to aversive visual associative learning (Gerber et a!., 2004). experiments. In the present study, we further explore sensory modalities for visual classical conditioning. We show that Drosophila larvae are Assay Plates, Light, Odors, and Reinforcer able to leam visual cues in many more different contexts than previously assumed. We established experimental paradigms using All experiments were performed with LED lamps (OSARAM mass assays in which larvae associate light information with LED, 80012 White), which illuminated the assay plates with white gustatory, olfactory, and electric shock stimuli. This allows a direct light of 760 lux from the top. The temperature was controlled comparison with recent studies on olfactory associative learning throughout all experiments between 22 and 23°C. Peb; dishes (Yarali, Hendel, & Gerber, 2006; Kaun, Hendel, Gerber, & (85-mm diameter; Greiner Bio-One GmbH, 4550 Kremsmeinster, Sokolowski, 2007; Honjo & Furukubo-Tokunaga, 2009; Pauls, Austria) were filled with a thin layer of agarose solution (2.5%; Pfitzenmaier, et aI., 2010; Pauls, Selcho, Gendre, Stocker, & . SIGMA Sigma-Aldrich, 9471 Buchs, Switzerland AS093-500G) Thum, 2010; Saumweber, Husse, & Gerber, 2011). As proof of boiled in a microwave oven. The plates were stored at room principle, we confirm that light can be used as CS and sugar as temperature and used the same day or on the following day. To rewarding reinforcer, as previously shown in single larva assays by keep one half or two quarters of a test plate in the darkness, the lid Gerber and coworkers (2004). Next, we demonstrate that high salt was covered with black tape. Depending on the learning paradigm, concentrations can trigger visual associative learning in an aver­ we added fructose (2M, FLUKA Sigma-Aldrich, 9471 Buchs, si ve gustatory learning paradigm. We further show that aversive Switzerland) or sodium chloride (J.5M, FLUKA Sigma-Aldrich, visual associative learning is not constrained to gustatory rein­ 9471 Buchs, Switzerland) to the agarose solution as a positive or forcement by successfully using electric shock as negative rein­ negative gustatory reinforcer, respectively. The olfactory learning forcement. Interestingly, we found that light itself can also be used paradigm was performed using 101-\-1 of either pure benzaldehyde as punishing US in olfactory learning, changing the preference for (BA, FLUKA Sigma-Aldrich, 9471 Buchs, Switzerland) or diluted one odorant after being paired with light. amylacetate (AM, FLUKA Sigma-Aldrich, 9471 Buchs, Switzer­ Thus, the same stimulus, namely light, can act as conditioned land, I :250 in paraffin oil, FLUKA Sigma-Aldrich, 9471 Buchs, and unconditioned stimulus in the classical conditioning procedure Switzerland) filled into custom-made Teflon containers of 4.5-mm of Drosophila larvae, raising the question of how reward, punish­ diameter with perforated lids, as described in Gerber and Stocker ment, and visual information is represented and converged within (2007). For the learning paradigm using electric shocks, we placed the neuronal circuit of the larval brain. The possibility to switch two semicircular copper electrodes of l-mm diameter and 70-mm between the different learning paradigms, together with the nu ­ length opposite to each other in the petri di sh. The electrodes were merical simplicity and functional amenability by genetic interven­ adjusted to the petri dish such that the di stance between them was tion of the larval visual circuit, provides an exceptional model to 5 cm at their ends and 7.5 cm in the middle. The electrodes were study the fundamental mechanisms of associative visual learning completely covered with a thin layer of agarose solution (2.5%), as and memory from the cellular up to the behavioral level. described in Pauls, Pfitzenmaier, et al. (2010). We used a variable isolating transformer (MUter RTT3, 0-270V AC, 2.5A, 675V A) to Method apply electric shocks. FLY Strains Preference Tests and Learning Experiments Preference tests. As indicated in Figure 2, preference tests Canton S wild-type strains were kept in mass culture at 25°C on were performed either on test plates where two quarters are dark standardized cornmeal medium under a l2-hr light-dark cycle. and two
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