In an attempt to correlate behavioral and neuronal changes, we examined the structural and functional effects of odor exposure in Drosophila. Young adult flies were exposed to a high concentration of the selected odor, usually benzaldehyde or isoamyl acetate, for 4 d and subsequently tested for their olfactory response to a variety of odorants and concentrations. The behavioral response showed specific adaptation to the exposed odor. By contrast, olfactory transduction, as measured in electroantennograms, remained normal. In vivo volume measurements were performed on olfactory glomeruli, the anatomical and functional units involved in odor processing. Preexposed flies exhibited volume reduction of certain glomeruli, in an odor-selective manner. Of a sample of eight glomeruli measured, dorsal medial (DM) 2 and ventral (V) were affected by benzaldehyde exposure, whereas DM6 was affected by isoamyl acetate. Estimation of the number of synapses indicates that volume reduction involves synapse loss that can reach 30% in the V glomerulus of flies adapted to benzaldehyde. Additional features of odorant-induced adaptation, including concentration dependence and perdurance, also show correlation, because both effects are elicited by high odor concentrations and are long-lasting (Ͼ1 week). Finally, the dunce mutant fails to develop behavioral adaptation as well as morphological changes in the olfactory glomeruli after exposure. These neural changes thus appear to require the cAMP signaling pathway. Key words: adaptation; olfactory glomeruli; memory; synapse number; dunce; DrosophilaA striking property of nervous systems is their ability to adapt structural and functional features to the input they receive during lifetime. Behavioral changes, including learning and memory, correlate with modulation of neuronal activity that can eventually lead to changes in gene expression and synapse number (Bailey and Kandel, 1993;Martin and Kandel, 1996;Milner et al., 1998;Corriveau, 1999;Yuste and Sur, 1999). Experience-related changes are usually detected in response to complex environments, however, making it difficult to establish a direct correlation between synapse modification and storage of specific information (for review, see Moser, 1999). The brain of the insect imago undergoes experience-dependent modifications (Bulloch and Ridgway, 1989). Integration centers such as the mushroom bodies (Heisenberg, 1998) and the central complex (Davis, 1996;Strausfeld, 1999) have been well studied in this respect (Brandon and Coss, 1982;Withers et al., 1993;Durst et al., 1994;Gronenberg et al., 1996;Barth and Heisenberg, 1997;Fahrbach et al., 1998;Barth, 1999). Additional brain structures also undergo behaviordependent changes, in particular the antennal lobes (AL), the insect olfactory centers (Masson and Mustaparta, 1990). In the honeybee, shifting to new behavioral tasks in the hive is accompanied by specific AL structural changes, albeit the triggering stimulus remains unknown (Winnington et al., 1996;Sigg et al., 1997).The relevance of...
The insect mushroom bodies (MBs) are paired brain centers which, like the mammalian hippocampus, have a prominent function in learning and memory. Despite convergent evidence for their crucial role in the formation and storage of associative memories, little is known about the mechanisms underlying such storage. In mammals and other species, the consolidation of stable memories is accompanied by structural plasticity involving variations in synapse number and/or size. Here, we address the question of whether the formation of olfactory long-term memory (LTM) could be associated with changes in the synaptic architecture of the MB networks. For this, we took advantage of the modular architecture of the honeybee MB neuropil, where synaptic contacts between olfactory input and MB neurons are segregated into discrete units (microglomeruli) which can be easily visualized and counted. We show that the density in microglomeruli increases as a specific olfactory LTM is formed, while the volume of the neuropil remains constant. Such variation is reproducible and is clearly correlated with memory consolidation, as it requires gene transcription. Thus stable structural synaptic rearrangements, including the growth of new synapses, seem to be a common property of insect and mammalian brain networks involved in the storage of stable memory traces.
Bee populations are declining in the industrialized world, raising concerns for the sustainable pollination of crops. Pesticides, pollutants, parasites, diseases, and malnutrition have all been linked to this problem. We consider here neurobiological, ecological, and evolutionary reasons why bees are particularly vulnerable to these environmental stressors. Central-place foraging on flowers demands advanced capacities of learning, memory, and navigation. However, even at low intensity levels, many stressors damage the bee brain, disrupting key cognitive functions needed for effective foraging, with dramatic consequences for brood development and colony survival. We discuss how understanding the relationships between the actions of stressors on the nervous system, individual cognitive impairments, and colony decline can inform constructive interventions to sustain bee populations.
Behavioural and cognitive processes play important roles in mediating an individual's interactions with its environment. Yet, while there is a vast literature on repeatable individual differences in behaviour, relatively little is known about the repeatability of cognitive performance. To further our understanding of the evolution of cognition, we gathered 44 studies on individual performance of 25 species across six animal classes and used meta-analysis to assess whether cognitive performance is repeatable. We compared repeatability () in performance (1) on the same task presented at different times (temporal repeatability), and (2) on different tasks that measured the same putative cognitive ability (contextual repeatability). We also addressed whether estimates were influenced by seven extrinsic factors (moderators): type of cognitive performance measurement, type of cognitive task, delay between tests, origin of the subjects, experimental context, taxonomic class and publication status. We found support for both temporal and contextual repeatability of cognitive performance, with mean estimates ranging between 0.15 and 0.28. Repeatability estimates were mostly influenced by the type of cognitive performance measures and publication status. Our findings highlight the widespread occurrence of consistent inter-individual variation in cognition across a range of taxa which, like behaviour, may be associated with fitness outcomes.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.
Complex external stimuli such as odorants are believed to be internally represented in the brain by spatiotemporal activity patterns of extensive neuronal ensembles. These activity patterns can be recorded by optical imaging techniques. However, optical imaging with conventional fluorescence dyes usually does not allow for resolving the activity of biologically defined groups of neurons. Therefore, specifically targeting reporter molecules to neuron populations of common genetic identity is an important goal. We report the use of the genetically encoded calcium-sensitive fluorescence protein cameleon 2.1 in the Drosophila brain. We visualized odorant-evoked intracellular calcium concentration changes in selectively labeled olfactory projection neurons both postsynaptically in the antennal lobe, the primary olfactory neuropil, and presynaptically in the mushroom body calyx, a structure involved in olfactory learning and memory. As a technical achievement, we show that calcium imaging with a genetically encoded fluorescence probe is feasible in a brain in vivo. This will allow one to combine Drosophila's advanced genetic tools with the physiological analysis of brain function. Moreover, we report for the first time optical imaging recordings in synaptic regions of the Drosophila mushroom body calyx and antennal lobe. This provides an important step for the use of Drosophila as a model system in olfaction.
Learning theories distinguish elemental from configural learning based on their different complexity. Although the former relies on simple and unambiguous links between the learned events, the latter deals with ambiguous discriminations in which conjunctive representations of events are learned as being different from their elements. In mammals, configural learning is mediated by brain areas that are either dispensable or partially involved in elemental learning. We studied whether the insect brain follows the same principles and addressed this question in the honey bee, the only insect in which configural learning has been demonstrated. We used a combination of conditioning protocols, disruption of neural activity, and optophysiological recording of olfactory circuits in the bee brain to determine whether mushroom bodies (MBs), brain structures that are essential for memory storage and retrieval, are equally necessary for configural and elemental olfactory learning. We show that bees with anesthetized MBs distinguish odors and learn elemental olfactory discriminations but not configural ones, such as positive and negative patterning. Inhibition of GABAergic signaling in the MB calyces, but not in the lobes, impairs patterning discrimination, thus suggesting a requirement of GABAergic feedback neurons from the lobes to the calyces for nonelemental learning. These results uncover a previously unidentified role for MBs besides memory storage and retrieval: namely, their implication in the acquisition of ambiguous discrimination problems. Thus, in insects as in mammals, specific brain regions are recruited when the ambiguity of learning tasks increases, a fact that reveals similarities in the neural processes underlying the elucidation of ambiguous tasks across species.learning | configural learning | mushroom bodies | honey bee | Apis mellifera
The storage of stable memories is generally considered to rely on changes in the functional properties and/or the synaptic connectivity of neural networks. However, these changes are not easily tractable given the complexity of the learning procedures and brain circuits studied. Such a search can be narrowed down by studying memories of specific stimuli in a given sensory modality and by working on networks with a modular and relatively simple organization. We have therefore focused on associative memories of individual odors and the possible related changes in the honeybee primary olfactory center, the antennal lobe (AL). As this brain structure is organized in well-identified morpho-functional units, the glomeruli, we looked for evidence of structural and functional plasticity in these units in relation with the bees' ability to store long-term memories (LTMs) of specific odors. Restrained bees were trained to form an odor-specific LTM in an appetitive Pavlovian conditioning protocol. The stability and specificity of this memory was tested behaviorally 3 d after conditioning. At that time, we performed both a structural and a functional analysis on a subset of 17 identified glomeruli by measuring glomerular volume under confocal microscopy, and odor-evoked activity, using in vivo calcium imaging. We show that long-term olfactory memory for a given odor is associated with volume increases in a subset of glomeruli. Independent of these structural changes, odor-evoked activity was not modified. Lastly, we show that structural glomerular plasticity can be predicted based on a putative model of interglomerular connections.[Supplemental material is available online at http: //www.learnmem.org.]In nature, animals' survival relies on their capacity to adapt to changes in the environment by constantly learning and memorizing novel information and modifying their behavior accordingly. This capacity relies on the long-term storage of learned information involving specific stable modifications of neural networks, both in their connectivity and in the strength of synaptic transmission (Matsuzaki 2007). For such long-term memory (LTM) to be specific for particular stimuli (for instance, an odor), they must rely on specific neural traces of these stimuli in the brain. A crucial question is whether such specific traces can be tracked down to individual neural units, given the complexity of the neuronal networks usually involved in the formation of LTM. Brain regions constituted of relatively few neurons and organized in clearly identified modules offer an excellent opportunity to answer this question. Among these is the insect antennal lobe (AL), an olfactory center that shares many similarities with the vertebrate olfactory bulb, but provides numerical simplicity. In the honeybee, the AL contains ;160 interconnected neuropil subunits, the glomeruli, which can be unambiguously identified across individuals (Galizia et al. 1999a). Experiments using in vivo calcium imaging have shown that glomeruli are functional units for odor...
The olfactory system of several holometabolous insect species undergoes anatomical changes after eclosion of the imago, following those occurring during metamorphosis. In parallel, odor experience and learning performance also evolve with age. Here, we analyze the case of adult Drosophila females. Synaptogenesis in the antennal lobe (AL) starts in late pupa and continues during the first days of adult life, at the same time as the behavioral response to odors matures. Individual olfactory glomeruli (DM6, DM2, and V) display specific growth patterns between days 1 and 12 of adult life. Experience can modify the olfactory pathway both structurally and functionally as shown by adaptation experiments. The modifications associated with this form of nonassociative learning seem to take place at a critical age. Exposure to benzaldehyde at days 2-5 of adult life, but not at 8-11, causes behavioral adaptation as well as structural changes in DM2 and V glomeruli. Altered levels in intracellular cAMP, caused by dunce and rutabaga mutants, do not affect the normal changes in glomerular size, at least at day 6 of development, but they prevent those elicited by experience, establishing a molecular difference between glomerular changes of intrinsic versus environmental origin. Taken together, these data demonstrate an imprinting-like phenomenon in the olfactory pathway of young Drosophila adults, and illustrate its glomerulus-specific dynamics.
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