Glutamate, GABA and Acetylcholine Signaling Components in the Lamina of the Drosophila Visual System

Abstract

Synaptic connections of neurons in the Drosophila lamina, the most peripheral synaptic region of the visual system, have been comprehensively described. Although the lamina has been used extensively as a model for the development and plasticity of synaptic connections, the neurotransmitters in these circuits are still poorly known. Thus, to unravel possible neurotransmitter circuits in the lamina of Drosophila we combined Gal4 driven green fluorescent protein in specific lamina neurons with antisera to γ-aminobutyric acid (GABA), glutamic acid decarboxylase, a GABAB type of receptor, L-glutamate, a vesicular glutamate transporter (vGluT), ionotropic and metabotropic glutamate receptors, choline acetyltransferase and a vesicular acetylcholine transporter. We suggest that acetylcholine may be used as a neurotransmitter in both L4 monopolar neurons and a previously unreported type of wide-field tangential neuron (Cha-Tan). GABA is the likely transmitter of centrifugal neurons C2 and C3 and GABAB receptor immunoreactivity is seen on these neurons as well as the Cha-Tan neurons. Based on an rdl-Gal4 line, the ionotropic GABAA receptor subunit RDL may be expressed by L4 neurons and a type of tangential neuron (rdl-Tan). Strong vGluT immunoreactivity was detected in α-processes of amacrine neurons and possibly in the large monopolar neurons L1 and L2. These neurons also express glutamate-like immunoreactivity. However, antisera to ionotropic and metabotropic glutamate receptors did not produce distinct immunosignals in the lamina. In summary, this paper describes novel features of two distinct types of tangential neurons in the Drosophila lamina and assigns putative neurotransmitters and some receptors to a few identified neuron types.

Mutation of theDrosophilavesicular GABA transporter disrupts visual figure detection

“…In the lamina, we observed labeled processes morphologically consistent with projections of the C2 cell type, previously proposed to contain GABA (Buchner et al, 1988;Datum et al, 1986). More recently, C3 also has been suggested to store GABA (Enell et al, 2007;Kolodziejczyk et al, 2008;Sinakevitch et al, 2003), and anti-dVGAT labeled C3-like processes in the lamina. In the medulla, tangential fibers expressed dVGAT (Fig.5D, arrow).…”

TheDrosophilaSK Channel (dSK) Contributes to Photoreceptor Performance by Mediating Sensitivity Control at the First Visual Network

“…In the proximal lamina, some of them formed lateral branches (Fig. 5F), characteristic of cholinergic L4 monopolar cells (Fischbach and Dittrich, 1989;Kolodziejczyk et al, 2008). In the medulla, the dSK antibody labeled axonal terminals of nonglutamatergic and, possibly, some overlapping glutamatergic neurons (Fig.…”

“…However, because the selected recordings to the given stimuli in Drosophila lamina had rather similar hyperpolarizing characteristics, all LMC data were analyzed together. Moreover, attributable to the smaller dimensions of L4 monopolar cell and their nonhistaminergic inputs (Kolodziejczyk et al, 2008), it is unlikely that any of the stable recordings (used in this study) would be from them.…”

“…5 D, H ). The AC and L2 interneu- rons were previously shown to be glutamate positive (Sinakevitch and Strausfeld, 2004;Kolodziejczyk et al, 2008;Raghu and Borst, 2011). We decorated glutamatergic neurons in the adult brain with a membrane GFP (UAS-mCD8GFP) using OK371-Gal4, an enhancer trap line inserted in the Drosophila vesicular glutamate transporter (DVGLUT) gene (Mahr and Aberle, 2006).…”

“…In the Drosophila lamina, histaminergic R1-R6 photoreceptors synapse (Hardie, 1987(Hardie, , 1989Gengs et al, 2002) onto the primary interneurons: the large monopolar cells (LMCs: L1-L3), and the amacrine cells (ACs) (Meinertzhagen and O'Neil, 1991;Uusitalo et al, 1995a). In turn, L2 and AC feedback onto photoreceptor terminals via excitatory inputs (Sinakevitch and Strausfeld, 2004;Kolodziejczyk et al, 2008). Upon light stimulation, photoreceptors depolarize while LMCs/ACs hyperpolarize (Shaw, 1984;Zheng et al, 2006), which thereby reduces excitatory feedback onto the photoreceptors.…”