Microglomerular Synaptic Complexes in the Sky-Compass Network of the Honeybee Connect Parallel Pathways from the Anterior Optic Tubercle to the Central Complex.

Martina Held,Ronja Hensgen,Annuska Berz,Keram Pfeiffer,Thomas S Muenz,Uwe Homberg,Wolfgang Rössler,Christina Scholl

doi:10.3389/fnbeh.2016.00186

Abstract

While the ability of honeybees to navigate relying on sky-compass information has been investigated in a large number of behavioral studies, the underlying neuronal system has so far received less attention. The sky-compass pathway has recently been described from its input region, the dorsal rim area (DRA) of the compound eye, to the anterior optic tubercle (AOTU). The aim of this study is to reveal the connection from the AOTU to the central complex (CX). For this purpose, we investigated the anatomy of large microglomerular synaptic complexes in the medial and lateral bulbs (MBUs/LBUs) of the lateral complex (LX). The synaptic complexes are formed by tubercle-lateral accessory lobe neuron 1 (TuLAL1) neurons of the AOTU and GABAergic tangential neurons of the central body’s (CB) lower division (TL neurons). Both TuLAL1 and TL neurons strongly resemble neurons forming these complexes in other insect species. We further investigated the ultrastructure of these synaptic complexes using transmission electron microscopy. We found that single large presynaptic terminals of TuLAL1 neurons enclose many small profiles (SPs) of TL neurons. The synaptic connections between these neurons are established by two types of synapses: divergent dyads and divergent tetrads. Our data support the assumption that these complexes are a highly conserved feature in the insect brain and play an important role in reliable signal transmission within the sky-compass pathway.

Highlights

Many insects have well developed abilities for orientation and navigation
We investigated the anatomy of large microglomerular synaptic complexes in the medial and lateral bulbs (MBUs/LBUs) of the lateral complex (LX)
We investigated the anatomy and ultrastructure of microglomerular synaptic complexes in the bulbs of the LX that connect the anterior optic tubercle (AOTU) to the central body (CB) in the brain of the honeybee Apis mellifera (Figure 1)

Summary

Introduction

Many insects have well developed abilities for orientation and navigation. En route, they rely on different strategies, like landmark navigation or vector integration (reviewed by Wehner, 2003; Menzel et al, 2006; Collett et al, 2013; Srinivasan, 2015). For spatial orientation many insects use sky-compass cues, like the position of the sun, the chromatic gradient and the polarization pattern of the sky (reviewed in Homberg et al, 2011). The neuronal basis and mechanisms underlying sky-compass orientation have been investigated anatomically and physiologically in a most detailed manner in locusts and crickets (reviewed by Homberg et al, 2011), whereas in honeybees, research into this topic is still at the beginning. The goal of this study is to investigate the anatomy of this pathway further from the LX into the central complex (CX), a neuropil which, amongst other functions, holds a neuronal representation of space around the animal (reviewed by Pfeiffer and Homberg, 2014)

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