Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera

Abstract

The honeybee, Apis mellifera, is a valuable model system for the study of olfactory coding and its learning and memory capabilities. In order to understand the synaptic organisation of olfactory information processing, the transmitter receptors of the antennal lobe need to be characterized. Using whole-cell patch-clamp recordings, we analysed the ligand-gated ionic currents of antennal lobe neurons in primary cell culture. Pressure applications of acetylcholine (ACh), gamma-amino butyric acid (GABA) or glutamate induced rapidly activating ionic currents. The ACh-induced current flows through a cation-selective ionotropic receptor with a nicotinic profile. The ACh-induced current is partially blocked by alpha-bungarotoxin. Epibatidine and imidacloprid are partial agonists. Our data indicate the existence of an ionotropic GABA receptor which is permeable to chloride ions and sensitive to picrotoxin (PTX) and the insecticide fipronil. We also identified the existence of a chloride current activated by pressure applications of glutamate. The glutamate-induced current is sensitive to PTX. Thus, within the honeybee antennal lobe, an excitatory cholinergic transmitter system and two inhibitory networks that use GABA or glutamate as their neurotransmitter were identified.

Homomeric RDL and Heteromeric RDL/LCCH3 GABA Receptors in the Honeybee Antennal Lobes: Two Candidates for Inhibitory Transmission in Olfactory Processing

“…However, similar observations were described in previous reports on pupal honeybee AL cells (Barbara et al 2005) and this apparent discrepancy could result from the activity of Na…”

“…Native neuronal ionotropic chlorideselective GABA receptors have been studied in several insect species such as fruitfly (Lee et al 2003;Su and O'Dowd 2003), cockroach (Alix et al 2002;Ihara et al 2005;Le Corronc and Hue 1999;Zhao et al 2003), cricket (Cayre et al 1999), sphinx moth (Sattelle et al 2003), and honeybee (Barbara et al 2005;Grünewald and Wersing 2008). Electrophysiological techniques and radioligand-binding assays have been used to compare the pharmacological profile of insect and vertebrate ionotropic GABA receptors, demonstrating that insect GABA receptors differ pharmacologically from their vertebrate counterparts (for review see .…”

“…Using immunocytochemical techniques, in addition to GABA other neurotransmitters such as acetylcholine, glutamate (for review see Bicker 1999), and histamine (Bornhauser and Meyer 1997) were identified in the ALs. Several lines of evidence indicate that not only GABA but also glutamate (Barbara et al 2005;El Hassani et al 2008) and histamine (Sachse et al 2006) can act as an inhibitory neurotransmitter in the honeybee brain.…”

A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing

“…In honey bees, the neonicotinoid imidacloprid inhibits receptors for -aminobutyric acid (GABA), a major neurotransmitter in the central nervous system (Thany, 2010). Imidacloprid is a partial agonist of nAChRs in brain areas associated with olfaction, learning and memory: cultured antennal lobe neurons (Barbara et al, 2005;Barbara et al, 2008) and cultured Kenyon cells from mushroom bodies (Déglise et al, 2002). Suchail et al found that imidacloprid is metabolized relatively quickly and has a half-life of 4-5h (Suchail et al, 2004a).…”

Acute Disruption of the NMDA Receptor Subunit NR1 in the Honeybee Brain Selectively Impairs Memory Formation

“…Interestingly, glutamate immunoreactivity, the localization of glutamate receptors and the recording of inhibitory and excitatory glutamate-induced currents, suggests the existence of a glutamate neurotransmission in the insect CNS (Ultsch et al, 1992;Cully et al, 1996;Barbara et al, 2005;Featherstone et al, 2005;Xia et al, 2005;Zannat et al, 2006;Devaud et al, 2008). In addition, several studies in the honeybee suggest that this neurotransmission is implicated in memory formation, but it is not known how it integrates the neural networks of olfactory coding and learning (Si et al, 2004;Locatelli et al, 2005;Kucharski et al, 2007;El Hassani et al, 2008).…”