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

Uwe Homberg,Monika Müller

doi:10.3389/fnbeh.2016.00230

Abstract

The central complex, a group of neuropils spanning the midline of the insect brain, plays a key role in spatial orientation and navigation. In the desert locust and other species, many neurons of the central complex are sensitive to the oscillation plane of polarized light above the animal and are likely involved in the coding of compass directions derived from the polarization pattern of the sky. Polarized light signals enter the locust central complex primarily through two types of γ-aminobutyric acid (GABA)-immunoreactive tangential neurons, termed TL2 and TL3 that innervate specific layers of the lower division of the central body (CBL). Candidate postsynaptic partners are columnar neurons (CL1) connecting the CBL to the protocerebral bridge (PB). Subsets of CL1 neurons are immunoreactive to antisera against locustatachykinin (LomTK). To better understand the synaptic connectivities of tangential and columnar neurons in the CBL, we studied its ultrastructural organization in the desert locust, both with conventional electron microscopy and in preparations immunolabeled for GABA or LomTK. Neuronal profiles in the CBL were rich in mitochondria and vesicles. Three types of vesicles were distinguished: small clear vesicles with diameters of 20–40 nm, dark dense-core vesicles (diameter 70–120 nm), and granular dense-core vesicles (diameter 70–80 nm). Neurons were connected via divergent dyads and, less frequently, through convergent dyads. GABA-immunoreactive neurons contained small clear vesicles and small numbers of dark dense core vesicles. They had both pre- and postsynaptic contacts but output synapses were observed more frequently than input synapses. LomTK immunostaining was concentrated on large granular vesicles; neurons had pre- and postsynaptic connections often with neurons assumed to be GABAergic. The data suggest that GABA-immunoreactive tangential neurons provide signals to postsynaptic neurons in the CBL, including LomTK-immunolabeled CL1 neurons, but in addition also receive input from LomTK-labeled neurons. Both types of neuron are additionally involved in local circuits with other constituents of the CBL.

Highlights

The central complex comprises a group of neuropils in the insect brain that extend across the brain midline
The field cricket, two species of dung beetle and the desert locust, neurons connecting the bulbs to the CBL, termed TL neurons, are sensitive to the plane of zenithal polarized light and constitute the principal input for sky compass signaling in the central complex (Vitzthum et al, 2002; Sakura et al, 2008; Heinze and Reppert, 2011; el Jundi et al, 2015)
In the fly Drosophila, homologous neurons to the ellipsoid body are sensitive to the azimuth of a vertical light bar, and likely provide spatial landmark information for head direction coding in the central complex (Seelig and Jayaraman, 2013, 2015)

Summary

INTRODUCTION

The central complex comprises a group of neuropils in the insect brain that extend across the brain midline. The field cricket, the desert locust and the monarch butterfly, neurons of the central complex are sensitive to the plane of dorsally presented polarized light and likely signal compass directions provided by the polarization pattern of the blue sky (Homberg et al, 2011; Heinze, 2014; el Jundi et al, 2015). 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) Two of these cell types, TL2 and TL3, comprising as many as 100 bilateral pairs of neurons, are immunoreactive to antisera against γ-aminobutyric acid (GABA; Figures 1B,E; Homberg et al, 1999). To further elucidate the synaptic organization at the input stage to the polarization vision network in the central complex, we investigated the ultrastructural organization of the CBL in the desert locust and analyzed the connectivities of GABA- and LomTK-immunoreactive neurons

MATERIALS AND METHODS

RESULTS

DISCUSSION

ETHICS STATEMENT