Modulation of transmitter release from the locust forewing stretch receptor neuron by GABAergic interneurons activated via muscarinic receptors

Abstract

The role of muscarinic receptors in the down‐regulation of acetylcholine (ACh) release from the locust forewing stretch receptor neuron (fSR) terminals has been investigated. Electrical stimulation of the fSR evokes monosynaptic excitatory postsynaptic potentials (EPSPs) in the first basalar motoneuron (BA1), produced mainly by the activation of postsynaptic nicotinic cholinergic receptors. The general muscarinic antagonists scopolamine (10−6 M) and atropine (10−8 to 10−6 M) caused a reversible increase in the amplitude of electrically evoked EPSPs. However, scopolamine (10−6 M) caused a slight depression in the amplitude of responses to ACh pressure‐applied to the soma of BA1. These observations indicate that the EPSP amplitude enhancement is due to the blockade of muscarinic receptors on neurons presynaptic to BA1. The muscarinic receptors may be located on the fSR itself and act as autoreceptors, and/or they may be located on GABAergic interneurons which inhibit ACh release from the fSR. Electron microscopical immunocytochemistry has revealed that GABA‐immunoreactive neurons make presynaptic inputs to the fSR. The GABA antagonist picrotoxin (10−6 M) caused a reversible increase in the EPSP amplitude, which does not appear to be due to an increase in sensitivity of BA1 to ACh, as picrotoxin (10−6 M) slightly decreased ACh responses recorded from BA1. Application of scopolamine (10−6 M) to a preparation preincubated with picrotoxin did not cause the EPSP amplitude enhancement normally seen in control experiments; in fact, it caused a slight depression. This indicates that at least some of the presynaptic muscarinic receptors are located on GABAergic interneurons that modulate transmission at the fSR/BA1 synapse. © 1999 John Wiley & Sons, Inc. J Neurobiol 40: 420–431, 1999

Two identified looming detectors in the locust: ubiquitous lateral connections among their inputs contribute to selective responses to looming objects

“…But ultrastructural evidence is still required before interposed inhibitory GABAergic neurons with mAChRs can be ruled out. GABAergic neurons with mAChRs, were found between the wing stretch receptor and a flight motoneuron that depresses the wing in the locust 47 . In the case of the LGMD 1 no GABA immunoreactive cells were interposed between the TmA boutons and their synapses with the LGMD 1.…”

Cholinergic calcium responses in cultured antennal lobe neurons of the migratory locust

“…Modulation of ACh release from synaptosome preparations provided biochemical evidence for muscarinic receptors in the CNS of locusts 40 , 41 . The gain of the monosynaptic connection between the cholinergic locust wing stretch receptor and an identified wing depressor motoneuron is modulated by muscarinic autoreceptors on the presynaptic terminals of the stretch receptor itself and/or on muscarinic receptors of GABAergic interneurons 42 , 43 . In intact Drosophila, muscarinic stimulation and blocking of mAChR diminish or enhance Ca 2+ transients of PN respectively during odor presentation 29 .…”

A Role for Sensory Inputs in the Generation of the Flight Motor Pattern

“…Recordings from rhythmically active preparations have also shown that the stretch receptor can modulate ongoing rhythmic activity in flight motor neurons (Pearson et al, 1983). The direct excitatory connection between the stretch receptor and the depressor motor neurons, which probably involves the release of several hundred vesicles during each excitatory post-synaptic potential, is modulated by octopamine and may also be modulated by pre-synaptic GABAergic inputs (Judge and Leitch, 1999;Simmons, 2001;Leitch et al, 2003). Yet these studies have not altered the role proposed by Burrows for the stretch receptor (Burrows, 1975).…”