Development and experience lead to increased volume of subcompartments of the honeybee mushroom body

doi:10.1016/S0163-1047(05)80025-1

Behavioral and Neural Biology

Volume 62, Issue 3, November 1994, Pages 259-263

https://doi.org/10.1016/S0163-1047(05)80025-1 Get rights and content

The mushroom bodies of insects are believed to be involved in higher order sensory integration and learning. In the honeybee, the mushroom body can be separated into three different, modality-specific input compartments and several morphologically inseparable output regions. By means of morphometric analysis we show that the volumes of these subcompartments depend on both the age of the adult bee and its experience. For the most part a significant, age-dependent increase in neuropile volume is observed. Additionally, the olfactory and visual input regions show expierence-related differences. Unlike other subcompartments, the visual input region does not change in volume with age, but only with experience. We thus suggest that experience is an important factor in the structural development of higher order brain regions of an insect, the honeybee.

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In insect brains, mushroom bodies are associated with memory and learning behavior. It has been demonstrated that the volume of the mushroom bodies in the brain of a worker honey bee changes during the adult stage. Changes in mushroom body volume imply high neuroplasticity in the brains and may be related to the age polyethism of honey bees. A suitable volume measurement method is needed to understand the correlation between behavioral changes and mushroom body volume changes in honey bees.
We developed a new protocol for insect micro-computed tomography by modifying a previously reported method. Permount™ mounting medium was used as the embedding medium for micro-computed tomography scanning.
This protocol can generate images with high contrast inside the brain and reduce the marked shape changes during specimen processing. From the resulting high-contrast images, we used freeware to generate a three-dimensional model and calculate the volumes of the mushroom bodies in honey bees. The measured volumes of the mushroom bodies were larger than the values reported in most previous studies. There was no significant difference between the left and right mushroom body volumes, but the volumes of honey bee mushroom bodies significantly increased with age.
Previous protocols for micro-computed tomography using dried samples would cause brain shrinkage; protocols using ethanol-preserved or resin-embedded samples generated images with lower contrast.
The embedding protocol for micro-computed tomography is suitable for calculating volume of the mushroom bodies in honey bee brains.
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Heliconius butterflies exhibit expanded mushroom bodies, a key brain region for learning and memory in insects, and a novel foraging strategy unique among Lepidoptera – traplining for pollen. We tested visual long-term memory across six Heliconius and outgroup Heliconiini species. Heliconius species exhibited greater fidelity to learned colors after eight days without reinforcement, with further evidence of recall at 13 days. We also measured the plastic response of the mushroom body calyces over this time period, finding substantial post-eclosion expansion and synaptic pruning in the calyx of Heliconius erato, but not in the outgroup Heliconiini Dryas iulia. In Heliconius erato, visual associative learning experience specifically was associated with a greater retention of synapses and recall accuracy was positively correlated with synapse number. These results suggest that increases in the size of specific brain regions and changes in their plastic response to experience may coevolve to support novel behaviors.
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Social animals often coordinate behavioural activities for the gathering, maintenance and protection of resources. In eusocial insects, morphological and/or behavioural heterogeneity among worker caste allows division of labour and, in some instances, the specialization of individuals in specific tasks. In leaf-cutting ants (genus Atta), the division of labour is based on body size differences (alloethism), meaning that differently sized workers will likely perform different tasks. Although alloethism is now well understood during foraging and processing of food resources in Atta, the relationship between body size and aggressive response has been poorly investigated, and, so far, it is not well understood how different morphological subcastes are integrated into the defensive strategy. Here, we quantified conspecifc and heterospecific aggression, in a within-colony social context (inside the nest), aiming to test which worker size class (subcaste) exhibits the most aggressive response against non-nestmates (NNMs). Workers were divided into three distinct subcastes, minors, majors and soldiers, and reared in subcolonies containing two individuals of each subcaste, as well as brood and the symbiotic fungus. We found a low probability of aggression towards conspecific NNMs and a high probability towards heterospecific NNMs. Quantification of aggression across subcastes showed that minors directed the most overt physical attacks towards heterospecific NNMs. We suggest that the nest, where minors perform most of their tasks, might constitute a strong social contextual stimulus for them, lowering their response threshold and increasing their aggression towards foreign ants. We also suggest that possible signals (i.e. chemical or mechanical) emitted during interactions involving minors stimulate larger workers to engage in fights, a mechanism that has been demonstrated in other ant species. The integration of size-specific behavioural traits might constitute a very efficient defensive mechanism.
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Visual navigation in ants has long been a focus of experimental study [1, 2, 3], but only recently have explicit hypotheses about the underlying neural circuitry been proposed [4]. Indirect evidence suggests the mushroom bodies (MBs) may be the substrate for visual memory in navigation tasks [5, 6, 7], while computational modeling shows that MB neural architecture could support this function [8, 9]. There is, however, no direct evidence that ants require MBs for visual navigation. Here we show that lesions of MB calyces impair ants’ visual navigation to a remembered food location yet leave their innate responses to visual cues unaffected. Wood ants are innately attracted to large visual cues, but we trained them to locate a food source at a specific angle away from such a cue. Subsequent lesioning of the MB calyces using procaine hydrochloride injection caused ants to revert toward their innate cue attraction. Handling and saline injection control ants still approached the feeder. Path straightness of lesioned and control ants did not differ from each other but was lower than during training. Reversion toward the cue direction occurred irrespective of whether the visual cue was ipsi- or contralateral to the lesion site, showing this is not due simply to an induced motor bias. Monocular occlusion did not diminish ants’ ability to locate the feeder, suggesting that MB lesions are not merely interrupting visual input to the calyx. The demonstrated dissociation between innate and learned visual responses provides direct evidence for a specific role of the MB in navigational memory.
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¹: We thank Dr. P. Stevenson for correcting the English. This work was supported by DFG grants (Pf 128/6)

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Behavioral and Neural Biology

References (21)

Learning and memory. A biological view

Rapid dendritic spine stem shortening during one-trial learning: the honeybee's first orientation flight

Brain Research

Physiological and anatomical properties of optical input fibers to the mushroom body in the bee brain

Journal of Insect Physiology

The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil

Neuron

Differential rearing effects on rat visual cortex synapses I. Synaptic and neuronal density and synapses per neuron

Brain Research

Are the structural changes in adult Drosophila mushroom bodies memory traces? Studies on biochemical learning mutants

Journal of Neurogenetics

Localization of shortterm memory in the brain of the bee

Apis mellifera. Physiology and Entomology

Functional roles of the mushroom bodies in insects

An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees

Nature

Drosophila mushroom body mutants are deficient in olfactory learning

Journal of Neurogenetics

Cited by (198)

Neuroplasticity in honey bee brains: An enhanced micro-computed tomography protocol for precise mushroom body volume measurement

Enhanced long-term memory and increased mushroom body plasticity in Heliconius butterflies

Small workers are more persistent fighters than soldiers in the highly polymorphic Atta leaf-cutting ants

Mushroom Bodies Are Required for Learned Visual Navigation, but Not for Innate Visual Behavior, in Ants

N<sup>6</sup>-methyladenosine modification of RNA controls dopamine synthesis to influence labour division in ants

Heliconiini butterflies as a case study in evolutionary cognitive ecology: behavioural innovation and mushroom body expansion