Abstract
Hymenoptera possess voluminous mushroom bodies (MBs), brain centres associated with sensory integration, learning and memory. The mushroom body input region (calyx) is organized in distinct synaptic complexes (microglomeruli, MG) that can be quantified to analyse body size-related phenotypic plasticity of synaptic microcircuits in these small brains. Leaf-cutting ant workers (Atta vollenweideri) exhibit an enormous size polymorphism, which makes them outstanding to investigate neuronal adaptations underlying division of labour and brain miniaturization. We particularly asked how size-related division of labour in polymorphic workers is reflected in volume and total numbers of MG in olfactory calyx subregions. Whole brains of mini, media and large workers were immunolabelled with anti-synapsin antibodies, and mushroom body volumes as well as densities and absolute numbers of MG were determined by confocal imaging and three-dimensional analyses. The total brain volume and absolute volumes of olfactory mushroom body subdivisions were positively correlated with head widths, but mini workers had significantly larger MB to total brain ratios. Interestingly, the density of olfactory MG was remarkably independent from worker size. Consequently, absolute numbers of olfactory MG still were approximately three times higher in large compared with mini workers. The results show that the maximum packing density of synaptic microcircuits may represent a species-specific limit to brain miniaturization.
Highlights
Many studies have investigated relationships between the volume of whole brains and/or particular brain centres and the behavioural repertoire, cognitive capacities, social life-style or food preference in a wide range of vertebrate and invertebrate species [1 –9]
Our key finding is that the maximum packing density of synaptic complexes (MG) does not differ in differently sized ant workers despite large differences in overall brain size and volumes of the mushroom bodies (MBs)
Anterograde tracing of projection neuron (PN) revealed the representation of olfactory and visual sensory input in subdivisions of the MB calyx in A. vollenweideri workers
Summary
Many studies have investigated relationships between the volume of whole brains and/or particular brain centres and the behavioural repertoire, cognitive capacities, social life-style or food preference in a wide range of vertebrate and invertebrate species [1 –9]. We analysed brains of highly polymorphic workers of A. vollenweideri at the level of synaptic complexes to address the question of how enormous body size differences associated with alloethism are reflected in the neuronal architecture of brain centres associated with higher order processing. Pure analyses of absolute and relative brain/neuropil volumes have been criticized [39,40], as it is the absolute number and complexity of neurons and their connectivity that affect neuronal processing capacities [39] We addressed this general issue of pure volume measurements by using immunolabelling of synaptic proteins and high-resolution confocal imaging to quantify and compare packing densities and absolute numbers of synaptic complexes and relate them to the absolute and relative volumes of the olfactory MB subdivisions. The head width (distance between the outer edges of the compound eyes) of workers was used as a measure for individual body size, and determined 2 using a calibrated scale (Wild, Gais, Switzerland) and a stereomicroscope at 25Â magnification (Wild M3Z). Graphs and figures were edited using COREL DRAW X3 (Corel Corporation Ltd., Ottawa, Canada), and, in some cases, adjusted for brightness and contrast
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