Recent studies have shown that the behavioral performance of adult honey bees is influenced by the temperature experienced during pupal development. Here we explore whether there are temperature-mediated effects on the brain. We raised pupae at different constant temperatures between 29 and 37°C and performed neuroanatomical analyses of the adult brains. Analyses focused on sensory-input regions in the mushroom bodies, brain areas associated with higher-order processing such as learning and memory. Distinct synaptic complexes [microglomeruli (MG)] within the mushroom body calyces were visualized by using fluorophoreconjugated phalloidin and an antibody to synapsin. The numbers of MG were different in bees that had been raised at different temperatures, and these differences persisted after the first week of adult life. In the olfactory-input region (lip), MG numbers were highest in bees raised at the temperature normally maintained in brood cells (34.5°C) and significantly decreased in bees raised at 1°C below and above this norm. Interestingly, in the neighboring visual-input region (collar), MG numbers were less affected by temperature. We conclude that thermoregulatory control of brood rearing can generate area-and modality-specific effects on synaptic neuropils in the adult brain. We propose that resulting differences in the synaptic circuitry may affect neuronal plasticity and may underlie temperature-mediated effects on multimodal communication and learning.I n honey bee colonies, brood temperature is controlled precisely within a temperature range of 33-36°C (1, 2). In the central brood area, fluctuations are as small as 35 Ϯ 0.5°C during the pupal period (3, 4). Exposure to strong deviations from normal brood temperatures is known to result in increased mortality and morphological deficits (1, 5). Environmentally induced temperature changes within the hive are compensated by individual honey bee workers via endothermic heat production or evaporation cooling (4, 6, 7). Thermoregulation during winter is achieved also by endothermic heat production, but with lower absolute temperatures and less precision compared with brood rearing in summer (8,9). A recent study demonstrated that the temperature experienced during pupal development influences the behavioral performance of adult bees (10). Worker bees that had been raised at lower temperatures (within the range of naturally occurring temperatures) performed less well in dance communication and olfactory learning than bees raised at higher temperatures.As in other holometabolous insects, postembryonic development in honey bees includes complete larval-adult metamorphosis. In the pupa, the larval nervous system becomes completely remodeled to accommodate the development of adultspecific sensory organs and motor systems, which are associated with the extraordinary changes in behavior. The hormonal and neuronal processes underlying this remarkable plasticity have been the subject of numerous studies, most of them performed on the sphinx moth (Manduca sexta) and...
To investigate the possible consequences of brood-temperature regulation in honey bee colonies on the quality of behavioral performance of adults, we placed honey bee pupae in incubators and allowed them to develop at temperatures held constant at 32°C, 34.5°C, and 36°C. This temperature range occurs naturally within hives. On emergence, the young adult bees were marked and introduced into foster colonies housed in normal and observation hives and allowed to live out their lives. No obvious difference in within-hive behavior was noted between the temperature-treated bees and the foster-colony bees. However, when the temperature-treated bees became foragers and were trained to visit a feeder 200 m from the hive, they exhibited clear differences in dance performance that could be correlated with the temperatures at which they had been raised: bees raised at 32°C completed only Ϸ20% of the dance circuits when compared with bees of the higher-temperature group. Also, the variance in the duration of the waggle phase is larger in 32°C-raised bees compared with 36°C-raised bees. All other parameters compared across all groups were not significantly different. One-trial learning and memory consolidation in the bees raised at different temperatures was investigated 1 and 10 min after conditioning the proboscis-extension reflex. Bees raised at 36°C performed as expected for bees typically classified as ''good learners,'' whereas bees raised at 32°C and 34.5°C performed significantly less well. We propose that the temperature at which pupae are raised will influence their behavioral performance as adults and may determine the tasks they carry out best inside and outside the hive. C ollective control of brood temperature is an essential aspect of the behavior of honey bees, and air temperatures measured close to the brood combs are, although never constant, always within a range of 33-36°C (1-7). High temperatures outside the hive are compensated by bringing water into the hive and evaporating this by wing fanning (8). Low temperatures inside the hive are compensated by the production of heat through thoracic muscle activity in individual bees, which then is transferred to the brood (9-11). Extended deviations from an optimal temperature window during development are known to result in morphological deficits (2,(12)(13)(14), so, by stabilizing the brood temperature, bees are able to control the influence of this environmental variable on the development of their offspring.Temperature regimes during the development of individual pupae, however, are dynamic and more complex than is implied by a single average air temperature (15). Measurements of the temperature within individual pupal cells, for example, revealed values that ranged from 32.6°C for the coldest pupa to 35.9°C for the warmest pupa. Taken over a 3-h period, the mean temperatures for these pupae were 33.7°C for the coldest and 35.0°C for the warmest pupa, but no pupae raised in the combs experienced a completely constant temperature (M. Kleinhenz, B. Bujok, S. Fu...
The mushroom bodies are high-order sensory integration centers in the insect brain. In the honeybee, their main sensory input regions are large, doubled calyces with modality-specific, distinct sensory neuropil regions. We investigated adult structural plasticity of input synapses in the microglomeruli of the olfactory lip and visual collar. Synapsin-immunolabeled whole-mount brains reveal that during the natural transition from nursing to foraging, a significant volume increase in the calycal subdivisions is accompanied by a decreased packing density of boutons from input projection neurons. To investigate the associated ultrastructural changes at pre- and postsynaptic sites of individual microglomeruli, we employed serial-section electron microscopy. In general, the membrane surface area of olfactory and visual projection neuron boutons increased significantly between 1-day-old bees and foragers. Both types of boutons formed ribbon and non-ribbon synapses. The percentage of ribbon synapses per bouton was significantly increased in the forager. At each presynaptic site the numbers of postsynaptic partners-mostly Kenyon cell dendrites-likewise increased. Ribbon as well as non-ribbon synapses formed mainly dyads in the 1-day-old bee, and triads in the forager. In the visual collar, outgrowing Kenyon cell dendrites form about 140 contacts upon a projection neuron bouton in the forager compared with only about 95 in the 1-day-old bee, resulting in an increased divergence ratio between the two stages. This difference suggests that synaptic changes in calycal microcircuits of the mushroom body during periods of altered sensory activity and experience promote behavioral plasticity underlying polyethism and social organization in honeybee colonies.
Insect mushroom bodies are critical for olfactory associative learning. We have carried out an extensive quantitative description of the synaptic organization of the calyx of adult Drosophila melanogaster, the main olfactory input region of the mushroom body. By using high-resolution confocal microscopy, electron microscopy-based three-dimensional reconstructions, and genetic labeling of the neuronal populations contributing to the calyx, we resolved the precise connections between large cholinergic boutons of antennal lobe projection neurons and the dendrites of Kenyon cells, the mushroom body intrinsic neurons. Throughout the calyx, these elements constitute synaptic complexes called microglomeruli. By single-cell labeling, we show that each Kenyon cell's claw-like dendritic specialization is highly enriched in filamentous actin, suggesting that this might be a site of plastic reorganization. In fact, Lim kinase (LimK) overexpression in the Kenyon cells modifies the shape of the microglomeruli. Confocal and electron microscopy indicate that each Kenyon cell claw enwraps a single bouton of a projection neuron. Each bouton is contacted by a number of such claw-like specializations as well as profiles of gamma-aminobutyric acid-positive neurons. The dendrites of distinct populations of Kenyon cells involved in different types of memory are partially segregated within the calyx and contribute to different subsets of microglomeruli. Our analysis suggests, though, that projection neuron boutons can contact more than one type of Kenyon cell. These findings represent an important basis for the functional analysis of the olfactory pathway, including the formation of associative olfactory memories.
Diversity in behavior plays a crucial role for the division of labor in insect societies. Social insects such as honeybees provide excellent model systems to investigate neuronal principles underlying behavioral plasticity. The two female castes, queens and workers, differ substantially in anatomy, physiology, aging and behavior. The different phenotypes are induced by environmental factors rather than genetic differences. Here we investigated environment- and age-dependent effects on the synaptic organization within higher order neuropils of the honeybee brain. Synaptic complexes (microglomeruli) in sensory-input regions of the mushroom bodies, prominent higher sensory integration centers, were analyzed quantitatively using fluorescent markers and confocal microscopy. Pre- and postsynaptic compartments of individual microglomeruli were labeled by anti-synapsin immunolabeling and f-actin detection with phalloidin in dendritic spines of mushroom-body intrinsic neurons. The results demonstrate that in queens the numbers of microglomeruli in the olfactory and visual input regions of the mushroom-body calyx are significantly lower than in workers. In queens raised in incubators, microglomeruli were affected by differences in pupal rearing temperature within the range of naturally occurring temperatures (32–36°C). The highest numbers of microglomeruli developed at a lower temperature compared to workers (33.5 vs. 34.5°C). We found a striking adult plasticity of microglomeruli numbers throughout the extended life-span of queens. Whereas microglomeruli in the olfactory lip increased with age (∼55%), microglomeruli in the visual collar significantly decreased (∼35%). We propose that developmental and adult plasticity of the synaptic circuitry in the mushroom-body calyx might underlie caste- and age-specific adaptations in behavior.
Honeybee workers express a pronounced age-dependent polyethism switching from various indoor duties to foraging outside the hive. This transition is accompanied by tremendous changes in the sensory environment that sensory systems and higher brain centers have to cope with. Foraging and age have earlier been shown to be associated with volume changes in the mushroom bodies (MBs). Using age- and task-controlled bees this study provides a detailed framework of neuronal maturation processes in the MB calyx during the course of natural behavioral maturation. We show that the MB calyx volume already increases during the first week of adult life. This process is mainly driven by broadening of the Kenyon cell dendritic branching pattern and then followed by pruning of projection neuron axonal boutons during the actual transition from indoor to outdoor duties. To further investigate the flexible regulation of division of labor and its neuronal correlates in a honeybee colony, we studied the modulation of the nurse-forager transition via a chemical communication system, the primer pheromone ethyl oleate (EO). EO is found at high concentrations on foragers in contrast to nurse bees and was shown to delay the onset of foraging. In this study, EO effects on colony behavior were not as robust as expected, and we found no direct correlation between EO treatment and synaptic maturation in the MB calyx. In general, we assume that the primer pheromone EO rather acts in concert with other factors influencing the onset of foraging with its effect being highly adaptive.
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