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

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.

GABA immunostaining in the central complex of dicondylian insects

“…In desert locusts, double labeling showed that two types of TL neurons, TL2 and TL3 are GABA‐immunoreactive (Homberg et al, ). Similar neurons have been identified in the field cricket (Sakura et al, 2008), the monarch butterfly (Heinze et al, ; Heinze & Reppert, ), a dung beetle (el Jundi et al, ), and two species of bees (Held et al, ; Stone et al, ). In the fruit fly, corresponding neurons were termed ring neurons (R‐neurons), based on their ring‐like innervation pattern in the ellipsoid body, and five subtypes R1–R5 were distinguished connecting the bulb with the ellipsoid body (Hanesch et al, 1989; Omoto et al, ).…”

“…Detailed analysis in the locust Schistocerca gregaria , the fly Drosophila melanogaster , and the moth Manduca sexta identified tangential neurons of the CBL (termed TL neurons in locusts, R neurons in flies) to be immunostained. These neurons have dendritic arborizations in microglomerular complexes in the bulbs, small areas in the lateral complex (Held et al, ; Schmitt, Stieb, Wehner, & Rössler, ; Träger, Wagner, Bausenwein, & Homberg, ). In addition, in all species studied, the CBU showed sparse GABA immunoreactivity.…”

Ultrastructure of GABA- and Tachykinin-Immunoreactive Neurons in the Lower Division of the Central Body of the Desert Locust

“…Signals are transferred via a specific pathway to the CBL (Homberg et al, 2003; Pfeiffer and Kinoshita, 2012; Held et al, 2016; Schmitt et al, 2016). In the desert locust, three types of tangential neuron to the CBL, termed TL1, TL2, and TL3 neurons provide polarization signals to the central complex (Vitzthum et al, 2002; Heinze et al, 2009).…”

The Topographical Mapping in Drosophila Central Complex Network and Its Signal Routing

“…If these neurons do not form synapses in both glomeruli, no information can be received or sent by the neurons. Therefore, axonal projections forming synapses with dendrites in the same glomerulus has become a basic assumption and has also been demonstrated in various Drosophila studies (Träger et al, 2008; Olsen et al, 2010; Held et al, 2016). It has also been shown in the central complex (Lin C.-Y.…”