Analysis of Synaptic Microcircuits in the Mushroom Bodies of the Honeybee

Abstract

Mushroom bodies (MBs) are multisensory integration centers in the insect brain involved in learning and memory formation. In the honeybee, the main sensory input region (calyx) of MBs is comparatively large and receives input from mainly olfactory and visual senses, but also from gustatory/tactile modalities. Behavioral plasticity following differential brood care, changes in sensory exposure or the formation of associative long-term memory (LTM) was shown to be associated with structural plasticity in synaptic microcircuits (microglomeruli) within olfactory and visual compartments of the MB calyx. In the same line, physiological studies have demonstrated that MB-calyx microcircuits change response properties after associative learning. The aim of this review is to provide an update and synthesis of recent research on the plasticity of microcircuits in the MB calyx of the honeybee, specifically looking at the synaptic connectivity between sensory projection neurons (PNs) and MB intrinsic neurons (Kenyon cells). We focus on the honeybee as a favorable experimental insect for studying neuronal mechanisms underlying complex social behavior, but also compare it with other insect species for certain aspects. This review concludes by highlighting open questions and promising routes for future research aimed at understanding the causal relationships between neuronal and behavioral plasticity in this charismatic social insect.

The brain of Cataglyphis ants: Neuronal organization and visual projections

“…Both LI and CO exhibit characteristic microglomerular structures (Figure 3e–g). Numerous microglomeruli in the visual (LI) and olfactory (CO) subregions of the MB calyx provide thousands of parallel microcircuits forming a rich neuronal substrate for memory formation (Stieb et al, 2012; for reviews, see Rössler, 2019; Groh & Rössler, 2020). In comparison to many other (mostly olfactory guided) ant species (Gronenberg, 1999, 2001), the visual CO is relatively prominent in the Cataglyphis MB (Figure 3d–g), further supporting the prominent role of vision.…”

Spatio-temporal Memory for Navigation in a Mushroom Body Model

“…The size of MB in our model (only 10,000 KCs) is smaller than for insect navigators (e.g. the honeybee mushroom body has about 368,000 KCs [8]). Also, our model does lifetime learning of all incoming information, with no selection or forgetting.…”

Plasticity and modulation of olfactory circuits in insects

“…The authors conclude that growth of new synapses may be involved in stable LTM in the insect brain, similar to what has been found in the mammalian brain (Abraham et al 2019 ). Compared with synaptic pruning following sensory exposure as described above, associative olfactory learning and the formation of transcription-dependent stable LTM resulted in a volume-independent increase of synaptic complexes in olfactory compartments of the honey bee MBs (Groh and Rössler 2020 ). This suggests that the increases in densities of synaptic boutons after associative LTM formation may represent a form of learning-related (Hebbian) structural plasticity in MB-calyx microcircuits.…”

“…Ethyl oleate is present at high concentrations on the cuticle of experienced foragers, sensed by OSNs on the antennae of nurse bees, processed in the AL (Muenz et al 2012 ), and finally causes a delay in adult behavioral maturation (Leoncini et al 2004 ). Future cohort experiments using more tightly controlled sensory manipulations and high-resolution anatomical and behavioral analyses are needed to dissect the changes in olfactory circuits caused by differences in sensory or social experience in order to find the mechanisms how they affect adult olfactory behavior (Groh and Rössler 2020 ). Winter bees (the last generation of bees in fall) might be a valuable model for studying adult olfactory plasticity in the future, as they live much longer than summer bees and start to resume foraging in the next spring after staying in the hive during the entire winter.…”

“…Olfaction is of particularly high importance in night- or dim-light active species and for social communication as in social insects. The multitude of available olfactory cues in the natural environment combined with limited size of the nervous system and the resulting neuronal processing capacities render neuronal plasticity and modulation as major factors to optimize the use of neural substrate (Dukas 2008 ; Gadenne et al 2016 ; Groh and Rössler 2020 ). However, the complexity of the nervous system can also set limits for behavioral and ecological plasticity (Bernays 2001 ).…”