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Timed and targeted differential regulation of nitric oxide synthase (NOS) and anti-NOS genes by reward conditioning leading to long-term memory formation

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posted on 2023-06-07, 23:39 authored by Sergei Korneev, Volko Straub, Ildiko KemenesIldiko Kemenes, Elena I Korneeva, Swidbert R Ott, Paul R Benjamin, Michael O'Shea
In a number of neuronal models of learning, signaling by the neurotransmitter nitric oxide (NO), synthesized by the enzyme neuronal NO synthase (nNOS), is essential for the formation of long-term memory (LTM). Using the molluscan model system Lymnaea, we investigate here whether LTM formation is associated with specific changes in the activity of members of the NOS gene family: Lym-nNOS1, Lym-nNOS2, and the antisense RNA-producing pseudogene (anti-NOS). We show that expression of the Lym-nNOS1 gene is transiently upregulated in cerebral ganglia after conditioning. The activation of the gene is precisely timed and occurs at the end of a critical period during which NO is required for memory consolidation. Moreover, we demonstrate that this induction of the Lym-nNOS1 gene is targeted to an identified modulatory neuron called the cerebral giant cell (CGC). This neuron gates the conditioned feeding response and is an essential part of the neural network involved in LTM formation. We also show that the expression of the anti-NOS gene, which functions as a negative regulator of nNOS expression, is downregulated in the CGC by training at 4 h after conditioning, during the critical period of NO requirement. This appears to be the first report of the timed and targeted differential regulation of the activity of a group of related genes involved in the production of a neurotransmitter that is necessary for learning, measured in an identified neuron of known function. We also provide the first example of the behavioral regulation of a pseudogene.

History

Publication status

  • Published

File Version

  • Published version

Journal

Journal of Neuroscience

ISSN

0270-6474

Publisher

Society for Neuroscience

Issue

5

Volume

25

Page range

1188-1192

Pages

5.0

Department affiliated with

  • Neuroscience Publications

Notes

First author. This paper was chosen for the This Week in the Journal. We report on timed training-provoked differential regulation of genes associated with the production of NO in a key modulatory neuron. Our findings provide a first demonstration of a pseudogene whose expression is regulated by a behavioral stimulus.

Full text available

  • Yes

Peer reviewed?

  • Yes

Legacy Posted Date

2012-02-06

First Open Access (FOA) Date

2016-03-22

First Compliant Deposit (FCD) Date

2016-08-17

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