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Nicotinic receptor activation induces NMDA receptor independent long-term potentiation of glutamatergic signalling in hippocampal oriens interneurons.

ABSTRACT:

Key points

Long-term potentiation of glutamatergic transmission to hippocampal interneurons in stratum oriens does not require NMDA receptors and the induction mechanisms are incompletely understood. Extracellular stimulation, conventionally used to monitor synaptic strength and induce long-term potentiation (LTP), does not exclusively recruit glutamatergic axons. We used optogenetic stimulation of either glutamatergic or cholinergic afferents to probe the relative roles of different signalling mechanisms in LTP induction. Selective stimulation of cholinergic axons was sufficient to induce LTP, which was prevented by chelating postsynaptic Ca²⁺ or blocking nicotinic receptors. The present study adds nicotinic receptors to the list of sources of Ca²⁺ that induce NMDA receptor independent LTP in hippocampal oriens interneurons.

Abstract

Many interneurons located in stratum oriens of the rodent hippocampus exhibit a form of long-term potentiation (LTP) of glutamatergic transmission that does not depend on NMDA receptors for its induction but, instead, requires Ca²⁺ -permeable AMPA receptors and group I metabotropic glutamate receptors. A role for cholinergic signalling has also been reported. However, electrical stimulation of presynaptic axons, conventionally used to evoke synaptic responses, does not allow the relative roles of glutamatergic and cholinergic synapses in the induction of LTP to be distinguished. Here, we show that repetitive optogenetic stimulation confined to cholinergic axons is sufficient to trigger a lasting potentiation of glutamatergic signalling. This phenomenon shows partial occlusion with LTP induced by electrical stimulation, and is sensitive to postsynaptic Ca²⁺ chelation and blockers of nicotinic receptors. ACh release from cholinergic axons is thus sufficient to trigger heterosynaptic potentiation of glutamatergic signalling to oriens interneurons in the hippocampus.

SUBMITTER: Nicholson E

PROVIDER: S-EPMC7839446 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Nicotinic receptor activation induces NMDA receptor independent long-term potentiation of glutamatergic signalling in hippocampal oriens interneurons.

Nicholson Elizabeth E Kullmann Dimitri M DM

The Journal of physiology 20201213 2

<h4>Key points</h4>Long-term potentiation of glutamatergic transmission to hippocampal interneurons in stratum oriens does not require NMDA receptors and the induction mechanisms are incompletely understood. Extracellular stimulation, conventionally used to monitor synaptic strength and induce long-term potentiation (LTP), does not exclusively recruit glutamatergic axons. We used optogenetic stimulation of either glutamatergic or cholinergic afferents to probe the relative roles of different sig ...[more]

PMID: 33251594

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Project description:The notion of functional interactions between the alpha7 nicotinic acetylcholine (alpha7 nACh) and the cannabinoid systems is emerging from recent in vitro and in vivo studies. Both the alpha7 nACh receptor and the cannabinoid receptor 1 (CB1) are highly expressed in the hippocampus. To begin addressing possible anatomical interactions between the alpha7 nACh and the cannabinoid systems in the rat hippocampus, we investigated the distribution of neurons expressing alpha7 nACh mRNA in relation to those containing CB1 mRNA. By in situ hybridization we found that the alpha7 nACh mRNA is diffusely expressed in principal neurons and is highly expressed in a subset of interneurons. We observed that the pattern of distribution of hippocampal interneurons co-expressing transcripts encoding alpha7 nACh and glutamate decarboxylase (GAD; synthesizing enzyme of GABA) closely resembles the one displayed by interneurons expressing CB1 mRNA. By double in situ hybridization we established that the majority of hippocampal interneurons expressing alpha7 nACh mRNA have high levels of CB1 mRNA. As CB1 interneurons contain cholecystokinin (CCK), we investigated the degree of cellular co-expression of alpha7 nACh mRNA and CCK, and found that the cellular co-existence of alpha7 nACh and CCK varies within the different layers of the hippocampus. In summary, we established that most of the hippocampal alpha7 nACh expressing interneurons are endowed with CB1 mRNA. We found that these alpha7 nACh/CB1 interneurons are the major subpopulation of hippocampal interneurons expressing CB1 mRNA. The alpha7 nACh expressing interneurons represent half of the detected population of CCK containing neurons in the hippocampus. Since it is well established that the vast majority of hippocampal interneurons expressing CB1 mRNA have 5-HT type 3 (5-HT3) receptors, we conclude that these hippocampal alpha7 nACh/5HT3/CB1/CCK interneurons correspond to those previously postulated to relay inputs from diverse cortical and subcortical regions about emotional, motivational, and physiological states.

Dataset Information

Nicotinic receptor activation induces NMDA receptor independent long-term potentiation of glutamatergic signalling in hippocampal oriens interneurons.

Key points

Abstract

Publications

Nicotinic receptor activation induces NMDA receptor independent long-term potentiation of glutamatergic signalling in hippocampal oriens interneurons.

Similar Datasets

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