Nicotinic potentiation of frog retinotectal transmission in tectum layer F by α3ß2, α4ß2, α2ß4, α6ß2, or α7 acetylcholine receptor subtypes.

OBJECTIVE: The aim of the study was to explore the effect of semi-specific antagonists and agonists of the nicotinic acetylcholine receptors on the paired-pulse facilitation and nicotinic tonic and phasic potentiation of the frog retinotectal synaptic transmission. MATERIALS AND METHODS: The experiments were performed in vivo on adult frogs, Rana temporaria. An individual retina ganglion cell (or its retinotectal fiber) was stimulated by current pulses delivered through multichannel stimulating electrode positioned on the retina. Responses to a discharge of a single retinal ganglion cell were recorded in the tectum by an extracellular carbon-fiber microelectrode positioned in the terminal arborization of the retinotectal fiber in the tectum layer F. The effect of the antagonists and agonists of the nicotinic acetylcholine receptors on the tectal responses has been tested. RESULTS: We found that the antagonists, MLA and DHßE, and agonists, RJR-2403 and choline, of the nicotinic acetylcholine receptors of the α3ß2, α4ß2, α2ß4, α6ß2 or α7 subtypes have had no effect on the phasic and tonic potentiation of the retinotectal transmission. The paired-pulse facilitation of the retinotectal transmission was not appreciably affected by the antagonists, but the choline, agonist of the α7 subtype receptor, has significantly decreased the paired-pulse facilitation. CONCLUSIONS: The tonic and phasic potentiation of the retinotectal transmission in the tectum layer F were not mediated by the receptors of α3ß2, α4ß2, α2ß4, α6ß2 or α7 subtype. The results suggest that presynaptic nicotinic acetylcholine receptors of the frog optic fibers are different from those of the mammalian optic fibers.

Phasic nicotinic potentiation of frog retinotectal transmission facilitates eliciting of higher activity level of the tectum column.

Nicotinic acetylcholine receptors contribute to the mediation of cholinergic role in attention, vigilance, orienting and detection of behavioral significant stimuli. We have recently demonstrated an increase of the intrinsic recurrent excitatory activity of the tectum column caused by the phasic (after-burst) nicotinic potentiation of a frog single axon retinotectal transmission to the tectum layer F. We have shown in the present study that the phasic nicotinic potentiation facilitates eliciting of higher activity level of the tectum column featured by generation of output signals from the tectum column. Since these signals can lead to an escape from danger reactions, a functional significance of nicotinic modulation of the neural network has been demonstrated. The phasic nicotinic potentiation that facilitates eliciting of higher activity level of the tectum column can be considered as a mechanism of vigilance and cue detection at the level of small neural network.

Phasic nicotinic potentiation of frog retinotectal transmission enhances intrinsic activity of tectum column.

It is well established that cholinergic modulation of functioning of neuronal networks is common in the central nervous system at all scales from neuronal columns to large nuclei. It is involved in various attentional, cognitive and behavioral performances. We have recently demonstrated that a frog retinotectal transmission exhibits after-burst (phasic) potentiation caused by activation of presynaptic nicotinic receptors. We show in the present study that the phasic potentiation of the retinotectal transmission enhances activity of the tectum column by increasing dendritic L-type calcium current, and excitation of recurrent pear-shaped neurons of the column. This enhancement lasts for tens of seconds and may provide the mechanism of animal alertness.

Frog retinal ganglion cells projecting to the tectum layer F release acetylcholine as co-mediator.

Neurons may release more than one classical neurotransmitter (co-mediator). It has been demonstrated in a recent study that a burst of action potentials in frog retina ganglion cells induces an after-burst increase (phasic potentiation) of the retinotectal transmission that lasts tens of seconds. This increase is mediated by presynaptic nicotinic acetylcholine receptors that are activated by the endogenous acetylcholine released during the burst of action potentials of the retinotectal fiber. The objective of the present study was to find out the origin of acetylcholine release. We show that reduction of the retinotectal transmission to the subthreshold level by application of moderate concentrations of kynurenic acid or CNQX had no effect on the phasic nicotinic potentiation of the retinotectal transmission. This demonstrates that the retinotectal terminals are the source of acetylcholine - responsible for the phasic potentiation of retinotectal transmission. The acetylcholine is thus co-released with glutamate.

Presynaptic nicotinic potentiation of a frog retinotectal transmission evoked by discharge of a single retina ganglion cell.

It was demonstrated in our previous studies of the frog retinotectal transmission that retinotectal synaptic potentials are enhanced by a factor of 1.5 due to the tonic presynaptic nicotinic potentiation, caused by the ambient level of the acetylcholine in the frog tectum. Furthermore, the results of those studies have indicated that the mechanism of the nicotinic potentiation is only partially exploited, because the application of the cholinergic agonist had increased the retinotectal transmission more than 2 times above the level of the tonic potentiation. The purpose of the present study was to explore this additional potentiation. We have shown that: (1) Bursts of 4-10 action potentials of a frog retina ganglion cell gave rise to an increase (phasic potentiation) of the retinotectal transmission 1.4-2.2 times, depending on the burst strength, that lasted tens of seconds. (2) This increase has been mediated through the presynaptic nicotinic acetylcholine receptors activated by the endogenous acetylcholine released into the tectum during relatively strong bursts of the retina ganglion cell. (3) Two types of the nicotinic acetylcholine receptors are co-localized in the presynaptic terminals of the individual retinotectal input to the tectum layer F--high-affinity (tonic) and low-affinity (phasic) nicotinic receptors.