Aversive bimodal associations impact visual and olfactory memory performance in Drosophila
Posted on: 9 August 2022 , updated on: 21 February 2023
Preprint posted on 23 July 2022
Article now published in iScience at http://dx.doi.org/10.1016/j.isci.2022.105485
If seeing is believing, then seeing and smelling is learning: memory in Drosophila with bimodal cues.
Selected by T. W. SchwanitzCategories: animal behavior and cognition, neuroscience
Updated 21 February 2023 with a postLight by Timothy W. Schwanitz
The preprint discussed here was recently published in iScience. It was a good article already in its preprint form, and so no major changes were necessary for publication. The new graphical abstract is one of the nicest additions to the publication, especially since it manages to boil down the complexity of the results into a relatively simple graphic. Some of the nuance and subtlety is preserved even in the simplified graphic, e.g., the preference wheels in the graphical abstract indicate partial preference in a way that is roughly proportional to the actual data. One cool result from the study that sadly did not make it into the abstract: the differences in the interactions between two senses in long-term bimodal memory vs short-term bimodal memory. Readers will have to dig deeper than the graphical abstract to learn about those interesting findings.
No new figures were added, though Figure 1 got split into two, and two panels were added to now Figure 2 to further clarify training paradigms. Some of the biggest changes to the paper were in the discussion, which now does an even better job of situating the broader impact of the findings (I smiled to see that the phrase “more the merrier” from my preLight made it into the discussion). The discussion of the final published paper is clearer and helps the reader better understand what is surprising in this study. The addition of a study limitations section also assists the reader in interpreting the results.
Background:
Think of a memorable place you have lived. Do you recall sights, sounds, smells, or maybe even textures and flavors? Memory often involves the complex integration of several senses. Many studies of the fruit fly Drosophila melanogaster have investigated their impressive olfactory learning abilities, or they have studied the fly’s visual system via color learning; however, not as many studies have looked at combinations of sensory inputs. When studied in isolation, fruit flies have often fared poorly in learning trials using color alone as a training cue (relative to their olfactory abilities, that is).
Thiagarajan and colleagues therefore investigated two sensory modalities, vision and olfaction, and their joint influence on learning. The researchers used a T-maze with four different stimuli: two food odors, acetoin and ethyl butyrate, as well as two different wavelengths of light, green and blue. The authors optimized the odor concentrations such that neither odor was inherently more attractive to the flies, and they did the same with light intensities. Flies were trained using the aversive stimulus of an electric shock in a training tube separate from the maze. The scientists used several different learning paradigms, all assessing how effectively the flies can recall the aversive association with either an odor or light stimulus—as measured by how many flies avoid the part of the T-maze with the aversive stimulus (see Fig. 1B of the preprint).
Fig. 1B. A schematic of the training tube that was used prior to the T-maze. Flies were exposed to an odor, a color of light, or a combination of both, while also being given an electric shock for one minute per round of training.
Key findings:
Flies are good at learning olfactory associations—but they are not as good at learning visual associations. The authors found no difference in avoidance between flies conditioned on an aversive olfactory stimulus in just one trial or in four trials. By contrast, a single learning trial was not sufficient to get a robust avoidance of the color of light associated with an aversive stimulus. After four learning trials, however, the flies did avoid the color of light associated with an aversive stimulus.
Having come to these conclusions, the researchers then did a series of tests where both an olfactory and a visual cue were used during the learning trials.
Olfactory cues improve visual memory; however, visual cues do not improve olfactory memory. If flies were trained on both an olfactory and a visual cue, but were then tested only on the visual cue, they performed better than if they were trained exclusively on visual cues; hence, olfactory cues augment visual memory. Nevertheless, flies trained on both cues but only tested on olfactory cues did just as well as flies trained only on olfactory cues. It appears that olfactory memories are already so strong that they cannot be enhanced by visual cues.
After these findings, the authors created a more complex learning environment where the flies were trained bimodally on all possible color and odor combinations. For example, acetoin and blue were presented together with an electric shock as the conditioned aversive stimulus, while ethyl butyrate and green were presented without a shock. The flies were then tested on only the visual or the olfactory cues.
Visual memory is improved by the addition of olfactory learning cues. In congruence with the previous experiments, flies that were trained with odors as well as colors learned to associate colors alone with a negative stimulus, while flies that only had colors did not form a significant visual memory. These results were confirmed by also using transgenic flies (i.e. olfactory mutants) that could not detect the odors used in the trial. Transgenic flies performed like flies that were trained only on colors, underscoring that visual memory formation is not very strong unless augmented by olfactory inputs.
Olfactory memory can be diminished by the addition of visual learning cues. Strikingly, though, flies that were trained on both colors and odors, and then tested only on odors, did not perform as well as flies that were only trained on odors. Adding a weak visual memory stimulus can actually reduce the strength of the olfactory memory.
The above results were all looking at short-term memory effects. As a final flourish to their study, Thiagarajan and colleagues added long-term versus short-term memory.
Long-term olfactory memory was improved by the presence of visual cues. In contrast to their short-term memory focused findings, adding a visual cue to olfactory learning improved long-term memory: more flies avoided the aversive stimulus. This result is especially interesting given that the flies had no detectable visual long-term memory, i.e., just using a visual stimulus after bimodal training did not result in significant levels of avoidance.
Why I think this study is important:
Memory is a complex process that involves time and many senses, so integrating multiple senses into experimental designs is an important step toward gaining a better understanding of how memory actually functions. The results in this preprint are especially fascinating because they show how memory is not a simple case of “the more the merrier.” Sometimes additional senses improve memory, as when the authors augmented visual cues with olfactory cues and then tested the flies in the short-term, or when the authors added visual cues to olfactory cues and tested the flies in the long-term. Other experiments in this study, however, showed that additional sensory cues weaken memory associations, as when the researchers added visual cues to olfactory cues and tested the flies in the short-term.
These complex results underscore the importance of testing assumptions like the idea that more sensory modalities always translate to better memory skills, or that findings at one temporal scale will hold true for all temporal scales.
doi: https://doi.org/10.1242/prelights.32464
Read preprintSign up to customise the site to your preferences and to receive alerts
Register hereAlso in the animal behavior and cognition category:
Pharyngeal neuronal mechanisms governing sour taste perception in Drosophila melanogaster
Matthew Davies
Precision Farming in Aquaculture: Use of a non-invasive, AI-powered real-time automated behavioural monitoring approach to predict gill health and improve welfare in Atlantic salmon (Salmo salar) aquaculture farms
Jasmine Talevi
Impaired 26S proteasome causes learning and memory deficiency and induces neuroinflammation mediated by NF-κB in mice
Gustavo Stelzer, Marcus Oliveira
Also in the neuroscience category:
Alzheimer’s Disease Patient Brain Extracts Induce Multiple Pathologies in Vascularized Neuroimmune Organoids for Disease Modeling and Drug Discovery
Manuel Lessi
Deciphering the nanoscale architecture of presynaptic actin using a micropatterned presynapse-on-glass model
Felipe Del Valle Batalla
The RNA binding protein HNRNPA2B1 regulates RNA abundance and motor protein activity in neurites
Felipe Del Valle Batalla
preListsanimal behavior and cognition category:
in the9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
List by | Martin Estermann |
Bats
A list of preprints dealing with the ecology, evolution and behavior of bats
List by | Baheerathan Murugavel |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
List by | Ana Dorrego-Rivas |
Also in the neuroscience category:
2024 Hypothalamus GRC
This 2024 Hypothalamus GRC (Gordon Research Conference) preList offers an overview of cutting-edge research focused on the hypothalamus, a critical brain region involved in regulating homeostasis, behavior, and neuroendocrine functions. The studies included cover a range of topics, including neural circuits, molecular mechanisms, and the role of the hypothalamus in health and disease. This collection highlights some of the latest advances in understanding hypothalamic function, with potential implications for treating disorders such as obesity, stress, and metabolic diseases.
List by | Nathalie Krauth |
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
List by | Alex Eve, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
List by | Alex Eve |
Journal of Cell Science meeting ‘Imaging Cell Dynamics’
This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.
List by | Helen Zenner |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
List by | Madhuja Samaddar et al. |
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
List by | Alex Eve |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
List by | Sandra Malmgren Hill |
Young Embryologist Network Conference 2019
Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London
List by | Alex Eve |