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Learning an olfactory discrimination task leads to heterogeneous results in honeybees with some bees performing very well and others at low rates. Here we investigated this behavioral heterogeneity and asked whether it was associated with particular gene expression patterns in the bee's brain. Bees were individually conditioned using a sequential conditioning protocol involving several phases of olfactory learning and retention tests. A cumulative score was used to differentiate the tested bees into high and low performers. The rate of CS+ odor learning was found to correlate most strongly with a cumulative performance score extracted from all learning and retention tests. Microarray analysis of gene expression in the mushroom body area of the brains of these bees identified a number of differentially expressed genes between high and low performers. These genes are associated with diverse biological functions, such as neurotransmission, memory formation, cargo trafficking and development.
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Comportamento Animal , Aprendizagem , Animais , Abelhas/genética , Abelhas/fisiologia , Comportamento Animal/fisiologia , Aprendizagem/fisiologia , Corpos Pedunculados/fisiologia , Corpos Pedunculados/metabolismo , Encéfalo/fisiologia , Encéfalo/metabolismo , Olfato/genética , Olfato/fisiologia , Odorantes , Perfilação da Expressão Gênica , Condicionamento Clássico/fisiologiaRESUMO
In his treatise on arthropod brains, Hans von Alten (1910) focuses on a specific functional group of insects-the flying Hymenoptera-which exhibit a spectrum of lifestyles ranging from solitary to social. His work presents a distinctive comparative neuro-anatomical approach rooted in an eco-evolutionary and eco-behavioral background. We regard his publication as an exceptionally valuable source of information and seek to inspire the research community dedicated to the study of the insect brain to explore its insights further, even after more than 110 years. We have translated and annotated his work, expecting it to engage researchers not just with its remarkable drawings but also with its substantive content and exemplary research strategy. The present text is designed to complement von Alten's publication, situating it within the temporal context of nineteenth-century and early twentieth-century studies, and to draw connections to contemporary perspectives, especially concerning a central brain structure: the mushroom body.
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Evolução Biológica , Encéfalo , Cognição , Himenópteros , Animais , Encéfalo/fisiologia , Encéfalo/anatomia & histologia , Cognição/fisiologia , História do Século XX , Himenópteros/fisiologia , Himenópteros/anatomia & histologia , História do Século XIX , Adaptação Fisiológica/fisiologia , Corpos Pedunculados/fisiologia , Corpos Pedunculados/anatomia & histologiaRESUMO
The study of navigation is informed by ethological data from many species, laboratory investigation at behavioural and neurobiological levels, and computational modelling. However, the data are often species-specific, making it challenging to develop general models of how biology supports behaviour. Wiener et al. outlined a framework for organizing the results across taxa, called the 'navigation toolbox' (Wiener et al. In Animal thinking: contemporary issues in comparative cognition (eds R Menzel, J Fischer), pp. 51-76). This framework proposes that spatial cognition is a hierarchical process in which sensory inputs at the lowest level are successively combined into ever-more complex representations, culminating in a metric or quasi-metric internal model of the world (cognitive map). Some animals, notably humans, also use symbolic representations to produce an external representation, such as a verbal description, signpost or map that allows communication of spatial information or instructions between individuals. Recently, new discoveries have extended our understanding of how spatial representations are constructed, highlighting that the hierarchical relationships are bidirectional, with higher levels feeding back to influence lower levels. In the light of these new developments, we revisit the navigation toolbox, elaborate it and incorporate new findings. The toolbox provides a common framework within which the results from different taxa can be described and compared, yielding a more detailed, mechanistic and generalized understanding of navigation.
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Cognição , Navegação Espacial , Humanos , Animais , Simulação por ComputadorRESUMO
Honeybees (Apis mellifera carnica) communicate the direction and distance to a food source by means of a waggle dance. We ask whether bees recruited by the dance use it only as a flying instruction, with the technical form of a polar vector, or also translate it into a location vector that enables them to set courses directed toward the food source from arbitrary locations within their familiar territory. The flights of recruits captured on exiting the hive and released at distant sites were tracked by radar. The recruits performed first a straight flight in approximately the compass direction indicated by the dance. However, this "vector" portion of their flights and the ensuing tortuous "search" portion were strongly and differentially affected by the release site. Searches were biased toward the true location of the food and away from the location specified by translating the origin for the danced polar vector to the release site. We conclude that by following the dance recruits get two messages, a polar flying instruction (bearing and range from the hive) and a location vector that enables them to approach the source from anywhere in their familiar territory. The dance communication is much richer than thought so far.
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Comunicação Animal , Esportes , Abelhas , Animais , Alimentos , ComunicaçãoRESUMO
Flying insects like the honeybee learn multiple features of the environment for efficient navigation. Here we introduce a novel paradigm in the natural habitat, and ask whether the memory of such features is generalized to novel test conditions. Foraging bees from colonies located in 5 different home areas were tested in a common area for their search flights. The home areas differed in the arrangements of rising natural objects or their lack, and in the existence or lack of elongated ground structures. The test area resembled partly or not at all the layout of landmarks in the respective home areas. In particular, the test area lacked rising objects. The search flights were tracked with harmonic radar and quantified by multiples procedures, extracting their differences on an individual basis. Random search as the only guide for searching was excluded by two model calculations. The frequencies of directions of flight sectors differed from both model calculations and between the home areas in a graded fashion. Densities of search flight fixes were used to create heat maps and classified by a partial least squares regression analysis. Classification was performed with a support vector machine in order to account for optimal hyperplanes. A rank order of well separated clusters was found that partly resemble the graded differences between the ground structures of the home areas and the test area. The guiding effect of elongated ground structures was quantified with respect to the sequence, angle and distance from these ground structures. We conclude that foragers generalize their specific landscape memory in a graded way to the landscape features in the test area, and argue that both the existence and absences of landmarks are taken into account. The conclusion is discussed in the context of the learning and generalization process in an insect, the honeybee, with an emphasis on exploratory learning in the context of navigation.
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Flying insects like the honeybee experience the world as a metric layout embedded in a compass, the time-compensated sun compass. The focus of the review lies on the properties of the landscape memory as accessible by data from radar tracking and analyses of waggle dance following. The memory formed during exploration and foraging is thought to be composed of multiple elements, the aerial pictures that associate the multitude of sensory inputs with compass directions. Arguments are presented that support retrieval and use of landscape memory not only during navigation but also during waggle dance communication. I argue that bees expect landscape features that they have learned and that are retrieved during dance communication. An intuitive model of the bee's navigation memory is presented that assumes the picture memories form a network of geographically defined locations, nodes. The intrinsic components of the nodes, particularly their generalization process leads to binding structures, the edges. In my view, the cognitive faculties of landscape memory uncovered by these experiments are best captured by the term cognitive map.
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Comunicação Animal , Aprendizagem , Abelhas , Animais , Comunicação , CogniçãoRESUMO
In this study we describe egfp expression induced by two techniques: in vivo electroporation and viral transduction in several cell types of the adult honeybee brain. Non-neuronal and neuronal cell types were identified and the expression persisted at least during three days. Kenyon cells, optic lobe neurons and protocerebral lobe neurons were electroporated. Astrocyte-like glia cells, fibrous lamellar glia cells and cortex glia cells were identified. Viral transduction targeted one specific type of glia cells that could not be identified. EGFP positive cells types were rather variable after electroporation, and viral transduction resulted in more homogenous groups of positive cells. We propose that these techniques remain a good alternative to transgenic animals because they potentially target only somatic cells.
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Eletroporação , Vetores Genéticos , Animais , Abelhas/genética , Encéfalo , Vetores Genéticos/genética , Neuroglia , NeurôniosRESUMO
The search strategy for the memory trace and its semantics is exemplified for the case of olfactory learning in the honeybee brain. The logic of associative learning is used to guide the experimental approach into the brain by identifying the anatomical and functional convergence sites of the conditioned stimulus and unconditioned stimulus pathways. Two of the several convergence sites are examined in detail, the antennal lobe as the first-order sensory coding area, and the input region of the mushroom body as a higher order integration center. The memory trace is identified as the pattern of associative changes on the level of synapses. The synapses are recruited, drop out, and change the transmission properties for both specifically associated stimulus and the non-associated stimulus. Several rules extracted from behavioral studies are found to be mirrored in the patterns of synaptic change. The strengths and the weaknesses of the honeybee as a model for the search for the memory trace are addressed in a comparison with Drosophila. The question is discussed whether the memory trace exists as a hidden pattern of change if it is not retrieved and whether an external reading of the content of the memory trace may ever be possible. Doubts are raised on the basis that the retrieval circuits are part of the memory trace. The concept of a memory trace existing beyond retrieval is defended by referring to two well-documented processes also in the honeybee, memory consolidation during sleep, and transfer of memory across brain areas.
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Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction are findable, accessible and reusable. To promote an open data culture, we have therefore developed the InsectBrainDatabase (IBdb), a free online platform for insect neuroanatomical and functional data. The IBdb facilitates biological insight by enabling effective cross-species comparisons, by linking neural structure with function, and by serving as general information hub for insect neuroscience. The IBdb allows users to not only effectively locate and visualize data, but to make them widely available for easy, automated reuse via an application programming interface. A unique private mode of the database expands the IBdb functionality beyond public data deposition, additionally providing the means for managing, visualizing, and sharing of unpublished data. This dual function creates an incentive for data contribution early in data management workflows and eliminates the additional effort normally associated with publicly depositing research data.
Insect neuroscience, like any field in the natural sciences, generates vast amounts of data. Currently, only a fraction are publicly available, and even less are reusable. This is because insect neuroscience data come in many formats and from many species. Some experiments focus on what insect brains look like (morphology), while others focus on how insect brains work (function). Some data come in the form of high-speed video, while other data contain voltage traces from individual neurons. Sharing is not as simple as uploading the raw files to the internet. To get a clear picture of how insect brains work, researchers need a way to cross-reference and connect different experiments. But, as it stands, there is no dedicated place for insect neuroscientists to share and explore such a diverse body of work. The community needs an open data repository that can link different types of data across many species, and can evolve as more data become available. Above all, this repository needs to be easy for researchers to use. To meet these specifications, Heinze et al. developed the Insect Brain Database. The database organizes data into three categories: species, brain structures, and neuron types. Within these categories, each entry has its own profile page. These pages bring different experiments together under one heading, allowing researchers to combine and compare data of different types. As researchers add more experiments, the profile pages will grow and evolve. To make the data easy to navigate, Heinze et al. developed a visual search tool. A combination of 2D and 3D images allow users to explore the data by anatomical location, without the need for expert knowledge. Researchers also have the option to upload their work in private mode, allowing them to securely share unpublished data. The Insect Brain Database brings data together in a way that is accessible not only to researchers, but also to students, and non-scientists. It will help researchers to find related work, to reuse existing data, and to build an open data culture. This has the potential to drive new discoveries combining research across the whole of the insect neuroscience field.
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Pesquisa Biomédica , Encéfalo/fisiologia , Bases de Dados Factuais , Gestão da Informação , Armazenamento e Recuperação da Informação , Insetos/fisiologia , Fenômenos Fisiológicos do Sistema Nervoso , Neurociências , Animais , Encéfalo/anatomia & histologia , Gráficos por Computador , Mineração de Dados , Insetos/anatomia & histologia , Internet , Interface Usuário-ComputadorRESUMO
Navigating animals combine multiple perceptual faculties, learn during exploration, retrieve multi-facetted memory contents, and exhibit goal-directedness as an expression of their current needs and motivations. Navigation in insects has been linked to a variety of underlying strategies such as path integration, view familiarity, visual beaconing, and goal-directed orientation with respect to previously learned ground structures. Most works, however, study navigation either from a field perspective, analyzing purely behavioral observations, or combine computational models with neurophysiological evidence obtained from lab experiments. The honey bee (Apis mellifera) has long been a popular model in the search for neural correlates of complex behaviors and exhibits extraordinary navigational capabilities. However, the neural basis for bee navigation has not yet been explored under natural conditions. Here, we propose a novel methodology to record from the brain of a copter-mounted honey bee. This way, the animal experiences natural multimodal sensory inputs in a natural environment that is familiar to her. We have developed a miniaturized electrophysiology recording system which is able to record spikes in the presence of time-varying electric noise from the copter's motors and rotors, and devised an experimental procedure to record from mushroom body extrinsic neurons (MBENs). We analyze the resulting electrophysiological data combined with a reconstruction of the animal's visual perception and find that the neural activity of MBENs is linked to sharp turns, possibly related to the relative motion of visual features. This method is a significant technological step toward recording brain activity of navigating honey bees under natural conditions. By providing all system specifications in an online repository, we hope to close a methodological gap and stimulate further research informing future computational models of insect navigation.
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As a canary in a coalmine warns of dwindling breathable air, the honeybee can indicate the health of an ecosystem. Honeybees are the most important pollinators of fruit-bearing flowers, and share similar ecological niches with many other pollinators; therefore, the health of a honeybee colony can reflect the conditions of a whole ecosystem. The health of a colony may be mirrored in social signals that bees exchange during their sophisticated body movements such as the waggle dance. To observe these changes, we developed an automatic system that records and quantifies social signals under normal beekeeping conditions. Here, we describe the system and report representative cases of normal social behavior in honeybees. Our approach utilizes the fact that honeybee bodies are electrically charged by friction during flight and inside the colony, and thus they emanate characteristic electrostatic fields when they move their bodies. These signals, together with physical measurements inside and outside the colony (temperature, humidity, weight of the hive, and activity at the hive entrance) will allow quantification of normal and detrimental conditions of the whole colony. The information provided instructs how to setup the recording device, how to install it in a normal bee colony, and how to interpret its data.
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Behavioural innovation and problem solving are widely considered to be important mechanisms by which animals respond to novel environmental challenges, including those induced by human activities. Despite their functional and ecological relevance, much of our current understanding of these processes comes from studies in vertebrates. Understanding of these processes in invertebrates has lagged behind partly because they are not perceived to have the cognitive machinery required. This perception is, however, challenged by recent evidence demonstrating sophisticated cognitive capabilities in insects despite their small brains. Here, we studied innovation, defined as the capacity to solve a new task, of a solitary bee (Osmia cornuta) in the laboratory by exposing naive individuals to an obstacle removal task. We also studied the underlying cognitive and non-cognitive mechanisms through a battery of experimental tests designed to measure associative learning, exploration, shyness and activity levels. We found that solitary bees can innovate, with 11 of 29 individuals (38%) being able to solve a new task consisting of lifting a lid to reach a reward. However, the propensity to innovate was uncorrelated with the measured learning capacity, but increased with exploration, boldness and activity. These results provide solid evidence that non-social insects can solve new tasks, and highlight the importance of interpreting innovation in the light of non-cognitive processes.
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Aprendizagem , Timidez , Animais , AbelhasRESUMO
Central place foraging insects like honeybees and bumblebees learn to navigate efficiently between nest and feeding site. Essential components of this behavior can be moved to the laboratory. A major component of navigational learning is the active exploration of the test arena. These conditions have been used here to search for neural correlates of exploratory walking in the central arena (ground), and thigmotactic walking in the periphery (slope). We chose mushroom body extrinsic neurons (MBENs) because of their learning-related plasticity and their multi-modal sensitivities that may code relevant parameters in a brain state-dependent way. Our aim was to test whether MBENs code space-related components or are more involved in state-dependent processes characterizing exploration and thigmotaxis. MBENs did not respond selectively to body directions or locations. Their spiking activity differently correlated with walking speed depending on the animals' locations: on the ground, reflecting exploration, or on the slope, reflecting thigmotaxis. This effect depended on walking speed in different ways for different animals. We then asked whether these effects depended on spatial parameters or on the two states, exploration and thigmotaxis. Significant epochs of stable changes in spiking did not correlate with restricted locations in the arena, body direction, or walking transitions between ground and slope. We thus conclude that the walking speed dependencies are caused by the two states, exploration and thigmotaxis, rather than by spatial parameters.
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Ongoing losses of pollinators are of significant international concern because of the essential role they have in our ecosystem, agriculture, and economy. Both chemical and non-chemical stressors have been implicated as possible contributors to their decline, but the increasing use of neonicotinoid insecticides has recently emerged as particularly concerning. In this study, honey bees were exposed orally to sublethal doses of the neonicotinoid clothianidin in the field in order to assess its effects on the foraging behavior, homing success, and dance communication. The foraging span and foraging activity at the contaminated feeder decreased significantly due to chronic exposure at field-realistic concentrations. Electrostatic field of dancing bees was measured and it was revealed that the number of waggle runs, the fanning time and the number of stop signals were significantly lower in the exposed colony. No difference was found in the homing success and the flight duration between control and treated bees released at a novel location within the explored area. However, a negative effect of the ambient temperature, and an influence of the location of the trained feeder was found. Finally, the residues of clothianidin accumulated in the abdomens of exposed foraging bees over time. These results show the adverse effects of a chronic exposure to sublethal doses of clothianidin on foraging and dance communication in honey bees.
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Comunicação Animal , Comportamento Apetitivo/efeitos dos fármacos , Abelhas/efeitos dos fármacos , Guanidinas/toxicidade , Inseticidas/toxicidade , Neonicotinoides/toxicidade , Tiazóis/toxicidade , Animais , Comportamento Alimentar/efeitos dos fármacosRESUMO
Sleep plays an essential role in both neural and energetic homeostasis of animals. Honey bees (Apis mellifera) manifest the sleep state as a reduction in muscle tone and antennal movements, which is susceptible to physical or chemical disturbances. This social insect is one of the most important pollinators in agricultural ecosystems, being exposed to a great variety of agrochemicals, which might affect its sleep behaviour. The intake of glyphosate (GLY), the herbicide most widely used worldwide, impairs learning, gustatory responsiveness and navigation in honey bees. In general, these cognitive abilities are linked with the amount and quality of sleep. Furthermore, it has been reported that animals exposed to sleep disturbances show impairments in both metabolism and memory consolidation. Consequently, we assessed the sleep pattern of bees fed with a sugar solution containing GLY (0, 25, 50 and 100 ng) by quantifying their antennal activity during the scotophase. We found that the ingestion of 50 ng of GLY decreased both antennal activity and sleep bout frequency. This sleep deepening after GLY intake could be explained as a consequence of the regenerative function of sleep and the metabolic stress induced by the herbicide.
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Glicina/análogos & derivados , Herbicidas/administração & dosagem , Sono/efeitos dos fármacos , Administração Oral , Animais , Antenas de Artrópodes/efeitos dos fármacos , Abelhas , Glicina/administração & dosagem , GlifosatoRESUMO
Evolutionary change is considered a major factor influencing the invasion of new habitats by plants. Yet, evidence on how such modifications promote range expansion remains rather limited. Here we investigated flower color modifications in the red poppy, Papaver rhoeas (Papaveraceae), as a result of its introduction into Central Europe and the impact of those modifications on its interactions with pollinators. We found that while flowers of Eastern Mediterranean poppies reflect exclusively in the red part of the spectrum, those of Central European poppies reflect both red and ultraviolet (UV) light. This change coincides with a shift from pollination by glaphyrid beetles (Glaphyridae) to bees. Glaphyrids have red-sensitive photoreceptors that are absent in bees, which therefore will not be attracted by colors of exclusively red-reflecting flowers. However, UV-reflecting flowers are easily detectable by bees, as revealed by visual modeling. In the North Mediterranean, flowers with low and high UV reflectance occur sympatrically. We hypothesize that Central European populations of P. rhoeas were initially polymorphic with respect to their flower color and that UV reflection drove a shift in the pollination system of P. rhoeas that facilitated its spread across Europe.
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The social behavior of honeybees (Apis mellifera) has been extensively investigated, but little is known about its neuronal correlates. We developed a method that allowed us to record extracellularly from mushroom body extrinsic neurons (MB ENs) in a freely moving bee within a small but functioning mini colony of approximately 1,000 bees. This study aimed to correlate the neuronal activity of multimodal high-order MB ENs with social behavior in a close to natural setting. The behavior of all bees in the colony was video recorded. The behavior of the recorded animal was compared with other hive mates and no significant differences were found. Changes in the spike rate appeared before, during or after social interactions. The time window of the strongest effect on spike rate changes ranged from 1 s to 2 s before and after the interaction, depending on the individual animal and recorded neuron. The highest spike rates occurred when the experimental animal was situated close to a hive mate. The variance of the spike rates was analyzed as a proxy for high order multi-unit processing. Comparing randomly selected time windows with those in which the recorded animal performed social interactions showed a significantly increased spike rate variance during social interactions. The experimental set-up employed for this study offers a powerful opportunity to correlate neuronal activity with intrinsically motivated behavior of socially interacting animals. We conclude that the recorded MB ENs are potentially involved in initiating and controlling social interactions in honeybees.
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The notion of the waggle dance simulating a flight towards a goal in a walking pattern has been proposed in the context of evolutionary considerations. Behavioral components, like its arousing effect on the social community, the attention of hive mates induced by this behavior, the direction of the waggle run relative to the sun azimuth or to gravity, as well as the number of waggles per run, have been tentatively related to peculiar behavioral patterns in both solitary and social insect species and are thought to reflect phylogenetic pre-adaptations. Here, I ask whether these thoughts can be substantiated from a functional perspective. Communication in the waggle dance is a group phenomenon involving the dancer and the followers that perform partially overlapping movements encoding and decoding the message respectively. It is thus assumed that the dancer and follower perform close cognitive processes. This provides us with access to these cognitive processes during dance communication because the follower can be tested in its flight performance when it becomes a recruit. I argue that the dance message and the landscape experience are processed in the same navigational memory, allowing the bee to fly novel direct routes, a property understood as an indication of a cognitive map.
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Neonicotinoids act as agonists on the nicotinic Acetylcholine receptor (nAChR) in insect brains, an essential molecular component of central brain structures involved in learning and memory formation. Sublethal doses might, therefore, impair neural processes necessary for adaptive experience dependent behaviour and thus reduce the fitness of pollinating insects on the individual and community level. First, the question was addressed whether clothianidin has an aversive taste for honey bees and concluded with both a laboratory and a semi-field experiment that bees are unable to distinguish between control and contaminated sucrose solutions. In the laboratory, proboscis extension response conditioning was performed with forager bees exposed to different concentrations of clothianidin (0.1, 0.3 and 0.8 ng/bee) before learning, after learning during memory consolidation, and just before memory retention. These tests at different timings allowed uncovering an impairment of the consolidation and retrieval of memory due to the exposure to clothianidin. It was concluded that an acute exposure to clothianidin has an adverse effect on memory processing in honey bees.
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Abelhas/fisiologia , Exposição Ambiental/efeitos adversos , Guanidinas/toxicidade , Inseticidas/toxicidade , Memória/efeitos dos fármacos , Neonicotinoides/toxicidade , Tiazóis/toxicidade , Animais , Comportamento Alimentar/efeitos dos fármacos , Aprendizagem/efeitos dos fármacos , Aprendizagem/fisiologia , Memória/fisiologia , Análise de Sobrevida , Percepção GustatóriaRESUMO
Cognitive impairments can be devastating for quality of life, and thus, preventing or counteracting them is of great value. To this end, the present study exploits the potential of the plant Rhodiola rosea and identifies the constituent ferulic acid eicosyl ester [icosyl-(2E)-3-(4-hydroxy-3-methoxyphenyl)-prop-2-enoate (FAE-20)] as a memory enhancer. We show that food supplementation with dried root material from R. rosea dose-dependently improves odor-taste reward associative memory scores in larval Drosophila and prevents the age-related decline of this appetitive memory in adult flies. Task-relevant sensorimotor faculties remain unaltered. From a parallel approach, a list of candidate compounds has been derived, including R. rosea-derived FAE-20. Here, we show that both R. rosea-derived FAE-20 and synthetic FAE-20 are effective as memory enhancers in larval Drosophila. Synthetic FAE-20 also partially compensates for age-related memory decline in adult flies, as well as genetically induced early-onset loss of memory function in young flies. Furthermore, it increases excitability in mouse hippocampal CA1 neurons, leads to more stable context-shock aversive associative memory in young adult (3-month-old) mice, and increases memory scores in old (>2-year-old) mice. Given these effects, and given the utility of R. rosea-the plant from which we discovered FAE-20-as a memory enhancer, these results may hold potential for clinical applications.