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      Aversive Bimodal Associations Differently Impact Visual and Olfactory Memory Performance in Drosophila

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          Summary

          Animals form sensory associations and store them as memories to guide behavioral decisions. Although unimodal learning has been studied extensively in insects, it is important to explore sensory cues in combination because most behaviors require multimodal inputs. In our study, we optimized the T-maze to employ both visual and olfactory cues in a classical aversive learning paradigm in Drosophila melanogaster. In contrast to unimodal training, bimodal training evoked a significant short-term visual memory after a single training trial. Interestingly, the same protocol did not enhance short-term olfactory memory and even had a negative impact. However, compromised long-lasting olfactory memory significantly improved after bimodal training. Our study demonstrates that the effect of bimodal integration on learning is not always beneficial and is conditional upon the formed memory strengths. We postulate that flies utilize information on a need-to basis: bimodal training augments weakly formed memories while stronger associations are impacted differently.

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          Highlights

          • Aversive olfactory memory is stronger and lasts longer than visual memory

          • Bimodal training with odor and color selectively improves short-term visual memory

          • Long-lasting, but not short-term, olfactory memory is enhanced by bimodal training

          • The value of bimodal sensory integration depends on the formed memory strength

          Abstract

          Behavioral neuroscience; Sensory neuroscience

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          Most cited references55

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          The neuronal architecture of the mushroom body provides a logic for associative learning

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            Genetic dissection of consolidated memory in Drosophila.

            Behavioral and pharmacological experiments in many animal species have suggested that memory is consolidated from an initial, disruptable form into a long-lasting, stable form within a few hours after training. We combined these traditional approaches with genetic analyses in Drosophila to show that consolidated memory of conditioned (learned) odor avoidance 1 day after extended training consisted of two genetically distinct, functionally independent memory components: anesthesia-resistant memory (ARM) and long-term memory (LTM). ARM decayed away within 4 days, was resistant to hypothermic disruption, was insensitive to the protein synthesis inhibitor cycloheximide (CXM), and was disrupted by the radish single-gene mutation. LTM showed no appreciable decay over 7 days, was sensitive to CXM, and was not disrupted by the radish mutation.
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              Visual acuity in insects.

              M F Land (1997)
              The acuity of compound eyes is determined by interommatidial angles, optical quality, and rhabdom dimensions. It is also affected by light levels and speed of movement. In insects, interommatidial angles vary from tens of degrees in Apterygota, to as little as 0.24 degrees in dragonflies. Resolution better than this is not attainable in compound eyes of realistic size. The smaller the interommatidial angle the greater the distance at which objects--prey, predators, or foliage--can be resolved. Insects with different lifestyles have contrasting patterns of interommatidial angle distribution, related to forward flight, capture on the wing, and predation on horizontal surfaces.
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                Author and article information

                Contributors
                Journal
                iScience
                iScience
                iScience
                Elsevier
                2589-0042
                03 November 2022
                22 December 2022
                03 November 2022
                : 25
                : 12
                : 105485
                Affiliations
                [1 ]Research Group Olfactory Coding, Max Planck Institute for Chemical Ecology, Jena, Germany
                [2 ]Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany
                [3 ]Max Planck Institute for Chemical Ecology, Jena, Germany
                Author notes
                []Corresponding author ssachse@ 123456ice.mpg.de
                [4]

                Senior author

                [5]

                Lead contact

                Article
                S2589-0042(22)01757-6 105485
                10.1016/j.isci.2022.105485
                9672954
                36404920
                eb3bce73-d9f5-4487-be0b-e8e0c505f549
                © 2022 The Author(s)

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 30 August 2022
                : 14 October 2022
                : 31 October 2022
                Categories
                Article

                behavioral neuroscience,sensory neuroscience
                behavioral neuroscience, sensory neuroscience

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