Neuroarchitecture of the central complex in the brain of the honeybee: Neuronal cell types

Abstract

The central complex (CX) in the insect brain is a higher order integration center that controls a number of behaviors, most prominently goal directed locomotion. The CX comprises the protocerebral bridge (PB), the upper division of the central body (CBU), the lower division of the central body (CBL), and the paired noduli (NO). Although spatial orientation has been extensively studied in honeybees at the behavioral level, most electrophysiological and anatomical analyses have been carried out in other insect species, leaving the morphology and physiology of neurons that constitute the CX in the honeybee mostly enigmatic. The goal of this study was to morphologically identify neuronal cell types of the CX in the honeybee Apis mellifera. By performing iontophoretic dye injections into the CX, we traced 16 subtypes of neuron that connect a subdivision of the CX with other regions in the bee's central brain, and eight subtypes that mainly interconnect different subdivisions of the CX. They establish extensive connections between the CX and the lateral complex, the superior protocerebrum and the posterior protocerebrum. Characterized neuron classes and subtypes are morphologically similar to those described in other insects, suggesting considerable conservation in the neural network relevant for orientation.

A projectome of the bumblebee central complex

“…Interestingly, bee PFL1,3 neurons only have a one column ipsilateral PB-FB projection offset ('PB-Shifted'; Figure 7, Figure 14a). Intracellular injection of a PFL1,3 cell revealed blebbed varicosities in the LAL and mixed branches in the FB, suggesting that this polarity is maintained across insects (Figure 7a; Hensgen et al, 2020). Although detailed analysis of the FB projection fields of these neurons will have to confirm the identical offset patterns for PFL1 and PFL3 cells, our data suggests that the PFL3 projection pattern of the fly does not exist in bees.…”

“…EPG/PEG cells arborized in the PB, the EB, and the gall (Figure 5a), while PENs sent projections through the PB, the EB, and a small compartment in the NO (NOs; Figure 6a-c). (Heinze and Homberg, 2008), and have been used in butterflies (Heinze et al, 2013), moths (de Vries et al, 2017, beetles (el Jundi et al, 2018), and bees (Stone et al, 2017;Hensgen et al, 2020 All FB columnar cells contained processes that arborized in both the PB and the FB. Several FB cell types sent projections towards the LX.…”

“…In flying insects, the paired NO are two spherical units situated ventrally in the CX, posterior to the CB (Figure 1c). In bees and flies, the NO receive mixed arborizations from PFN and PEN cells, which propagate signals to and from the CB and PB columns in the contralateral hemisphere, as well as input from large tangential cells (Figure 4, Figure 6c; Stone et al, 2017;Hensgen et al, 2020;Hadeln et al, 2020;Hulse et al, 2020).…”

“…Importantly, the majority of these cell types have known homologues in other insects. These include EPG/PEGs, PENs, PFNs, hΔs, and putative motor output cells, PFL1,3 and PFL2 (Homberg, 1985;Heinze and Homberg, 2008;Heinze et al, 2013;Wolff et al, 2015;Stone et al, 2017;el Jundi et al, 2018;Hensgen et al, 2020). Drawing comparisons to the fly data, we can distinguish four different categories of cross species resemblance:…”

“…The copyright holder for this preprint this version posted March 29, 2021. ; https://doi.org/10.1101/2021.03.26.437137 doi: bioRxiv preprint shown to facilitate the encoding of self-motion cues, with anatomical homologues having been identified across insect species (Heinze and Homberg, 2008;Heinze et al, 2013;Wolff et al, 2015;Stone et al, 2017;el Jundi et al, 2018;Hadeln et al, 2020;Hensgen et al, 2020). These include PFN, PEN, and LNO tangential cells (Figure 4e-f).…”