Volume and density of microglomeruli in the honey bee mushroom bodies do not predict performance on a foraging task

Nest, Byron N. Van; Wagner, Ashley E.; Marrs, Glen S.; Fahrbach, Susan E.

doi:10.1002/dneu.22492

Cited by 14 publications

(13 citation statements)

References 97 publications

(142 reference statements)

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“…In fruit flies, visual reversal learning has also been shown to be improved by GABAergic inhibition [ 54 ], suggesting that sparse coding might be beneficial to solve this task. In honey bees, the density of synaptic boutons in the collar was not related to performance in a 2-colour discrimination task [ 55 ], but bumblebees with a high density of synaptic boutons in the collar have been shown to learn faster to discriminate between 10 different colours [ 56 ]. A possibility might be that increasing number of synaptic boutons in honey bees with greater experience might facilitate some learning tasks (not tested here) to the expense of others (such as reversal learning).…”

Section: Discussionmentioning

confidence: 99%

Relationship between brain plasticity, learning and foraging performance in honey bees

et al. 2018

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Brain structure and learning capacities both vary with experience, but the mechanistic link between them is unclear. Here, we investigated whether experience-dependent variability in learning performance can be explained by neuroplasticity in foraging honey bees. The mushroom bodies (MBs) are a brain center necessary for ambiguous olfactory learning tasks such as reversal learning. Using radio frequency identification technology, we assessed the effects of natural variation in foraging activity, and the age when first foraging, on both performance in reversal learning and on synaptic connectivity in the MBs. We found that reversal learning performance improved at foraging onset and could decline with greater foraging experience. If bees started foraging before the normal age, as a result of a stress applied to the colony, the decline in learning performance with foraging experience was more severe. Analyses of brain structure in the same bees showed that the total number of synaptic boutons at the MB input decreased when bees started foraging, and then increased with greater foraging intensity. At foraging onset MB structure is therefore optimized for bees to update learned information, but optimization of MB connectivity deteriorates with foraging effort. In a computational model of the MBs sparser coding of information at the MB input improved reversal learning performance. We propose, therefore, a plausible mechanistic relationship between experience, neuroplasticity, and cognitive performance in a natural and ecological context.

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Section: Discussionmentioning

confidence: 99%

Relationship between brain plasticity, learning and foraging performance in honey bees

et al. 2018

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“…Van Nest et al . [ 28 ] found no correlation between microglomerular density in the mushroom body calyces and honeybee performance on a two-colour visual discrimination task. In our study, we found a statistically strong positive correlation between performance on a visual discrimination task and microglomerular density in the mushroom body calyxes, and specifically in the visual input region (collar region).…”

Section: Discussionmentioning

confidence: 99%

“…In our study, we found a statistically strong positive correlation between performance on a visual discrimination task and microglomerular density in the mushroom body calyxes, and specifically in the visual input region (collar region). The reason for the difference in sign of correlation (with [ 28 ]) and significance (with [ 29 ]) may be owing to the differences in controls, as we controlled for both age and prior foraging experience. In addition, the 10-colour Learning task in our experiment was arguably more difficult than the traditional Two-colour Learning task used by these other studies.…”

Section: Discussionmentioning

confidence: 99%

“…Recent work also showed that establishment of long-term memory is accompanied by changes in microglomerular density within the mushroom body of the insect brain, but this has only been examined for olfactory learning [ 25 , 26 ]. The few studies exploring how visual information affects microglomeruli in the insect brain have been limited to light exposure or deprivation [ 21 , 24 , 27 ], or a simple two-colour discrimination task (see [ 28 , 29 ] and Discussion). Understanding how individual learning abilities might relate to neural architecture will provide valuable information on the neural underpinnings of cognition in general.…”

Section: Introductionmentioning

confidence: 99%

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A possible structural correlate of learning performance on a colour discrimination task in the brain of the bumblebee

MaBouDi

Egertová

et al. 2017

Proc. R. Soc. B.

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Synaptic plasticity is considered to be a basis for learning and memory. However, the relationship between synaptic arrangements and individual differences in learning and memory is poorly understood. Here, we explored how the density of microglomeruli (synaptic complexes) within specific regions of the bumblebee (Bombus terrestris) brain relates to both visual learning and inter-individual differences in learning and memory performance on a visual discrimination task. Using whole-brain immunolabelling, we measured the density of microglomeruli in the collar region (visual association areas) of the mushroom bodies of the bumblebee brain. We found that bumblebees which made fewer errors during training in a visual discrimination task had higher microglomerular density. Similarly, bumblebees that had better retention of the learned colour-reward associations two days after training had higher microglomerular density. Further experiments indicated experience-dependent changes in neural circuitry: learning a colour-reward contingency with 10 colours (but not two colours) does result, and exposure to many different colours may result, in changes to microglomerular density in the collar region of the mushroom bodies. These results reveal the varying roles that visual experience, visual learning and foraging activity have on neural structure. Although our study does not provide a causal link between microglomerular density and performance, the observed positive correlations provide new insights for future studies into how neural structure may relate to inter-individual differences in learning and memory.

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“…However, with brood exposed workers ( pre-eclosion) also being affected this indicates exposure to be affecting synaptic development and proliferation in the calyces. For instance, microglomeruli configuration is considered to be associated with learning and memory in bees [73][74][75][76], and reduced density from neonicotinoid exposure has been reported in honeybees [35]. It could also stem from impeded neurogenesis where neuronal precursor cells were prevented from giving rise to mushroom body Kenyon cells, which in honeybees occurs during development pre-eclosion [77,78], or reduced Kenyon cell size as shown in neonicotinoid exposure experiments on bumblebee cell cultures [79].…”

Section: (A) Pesticide Exposure During Early Development Affected Resmentioning

confidence: 99%

Insecticide exposure during brood or early-adult development reduces brain growth and impairs adult learning in bumblebees

et al. 2020

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For social bees, an understudied step in evaluating pesticide risk is how contaminated food entering colonies affects residing offspring development and maturation. For instance, neurotoxic insecticide compounds in food could affect central nervous system development predisposing individuals to become poorer task performers later-in-life. Studying bumblebee colonies provisioned with neonicotinoid spiked nectar substitute, we measured brain volume and learning behaviour of 3 or 12-day old adults that had experienced in-hive exposure during brood and/or early-stage adult development. Micro-computed tomography scanning and segmentation of multiple brain neuropils showed exposure during either of the developmental stages caused reduced mushroom body calycal growth relative to unexposed workers. Associated with this was a lower probability of responding to a sucrose reward and lower learning performance in an olfactory conditioning test. While calycal volume of control workers positively correlated with learning score, this relationship was absent for exposed workers indicating neuropil functional impairment. Comparison of 3-and 12-day adults exposed during brood development showed a similar degree of reduced calycal volume and impaired behaviour highlighting lasting and irrecoverable effects from exposure despite no adult exposure. Our findings help explain how the onset of pesticide exposure to whole colonies can lead to lag-effects on growth and resultant dysfunction.

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Volume and density of microglomeruli in the honey bee mushroom bodies do not predict performance on a foraging task

Cited by 14 publications

References 97 publications

Relationship between brain plasticity, learning and foraging performance in honey bees

Relationship between brain plasticity, learning and foraging performance in honey bees

A possible structural correlate of learning performance on a colour discrimination task in the brain of the bumblebee

Insecticide exposure during brood or early-adult development reduces brain growth and impairs adult learning in bumblebees

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