How nitric oxide helps update memories

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Abstract

Some dopaminergic neurons release both dopamine and nitric oxide to increase the flexibility of olfactory memories.

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Behavioral consequences of dopamine deficiency in the Drosophila central nervous system.

Kazuhiko Kume, Serge Birman, Thomas Preat … (2011)

The neuromodulatory function of dopamine (DA) is an inherent feature of nervous systems of all animals. To learn more about the function of neural DA in Drosophila, we generated mutant flies that lack tyrosine hydroxylase, and thus DA biosynthesis, selectively in the nervous system. We found that DA is absent or below detection limits in the adult brain of these flies. Despite this, they have a lifespan similar to WT flies. These mutants show reduced activity, extended sleep time, locomotor deficits that increase with age, and they are hypophagic. Whereas odor and electrical shock avoidance are not affected, aversive olfactory learning is abolished. Instead, DA-deficient flies have an apparently "masochistic" tendency to prefer the shock-associated odor 2 h after conditioning. Similarly, sugar preference is absent, whereas sugar stimulation of foreleg taste neurons induces normal proboscis extension. Feeding the DA precursor L-DOPA to adults substantially rescues the learning deficit as well as other impaired behaviors that were tested. DA-deficient flies are also defective in positive phototaxis, without alteration in visual perception and optomotor response. Surprisingly, visual tracking is largely maintained, and these mutants still possess an efficient spatial orientation memory. Our findings show that flies can perform complex brain functions in the absence of neural DA, whereas specific behaviors involving, in particular, arousal and choice require normal levels of this neuromodulator.

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A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP.

V Lev, Roger Y. Tsien, Victoria Wong … (2002)

Long-term depression (LTD) at cerebellar parallel fiber (PF)-Purkinje cell synapses must be balanced by long-term potentiation (LTP) to prevent saturation and allow reversal of motor learning. The only previously analyzed form of cerebellar LTP is induced by 4-8 Hz PF stimulation and requires cAMP but not nitric oxide. It is a poor candidate to reverse LTD because it is presynaptically expressed whereas LTD is postsynaptic. We now characterize a new form of LTP induced by 1 Hz PF stimulation for at least 300 s. This LTP is postsynaptically expressed, enhanced by chelating postsynaptic Ca(2+), and depends on nitric oxide but not cAMP or cGMP, making it a plausible anti-Hebbian counterpart to Hebbian LTD.

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Are mushroom bodies cerebellum-like structures?

Sarah M Farris (2011)

The mushroom bodies are distinctive neuropils in the protocerebral brain segments of many protostomes. A defining feature of mushroom bodies is their intrinsic neurons, masses of cytoplasm-poor globuli cells that form a system of lobes with their densely-packed, parallel-projecting axon-like processes. In insects, the role of the mushroom bodies in olfactory processing and associative learning and memory has been studied in depth, but several lines of evidence suggest that the function of these higher brain centers cannot be restricted to these roles. The present account considers whether insight into an underlying function of mushroom bodies may be provided by cerebellum-like structures in vertebrates, which are similarly defined by the presence of masses of tiny granule cells that emit thin parallel fibers forming a dense molecular layer. In vertebrates, the shared neuroarchitecture of cerebellum-like structures has been suggested to underlie a common functional role as adaptive filters for the removal of predictable sensory elements, such as those arising from reafference, from the total sensory input. Cerebellum-like structures include the vertebrate cerebellum, the electrosensory lateral line lobe, dorsal and medial octavolateral nuclei of fish, and the dorsal cochlear nucleus of mammals. The many architectural and physiological features that the insect mushroom bodies share with cerebellum-like structures suggest that it might be fruitful to consider mushroom body function in light of a possible role as adaptive sensory filters. The present account thus presents a detailed comparison of the insect mushroom bodies with vertebrate cerebellum-like structures. Copyright © 2011 Elsevier Ltd. All rights reserved.

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Andrew C Lin:

ORCID: https://orcid.org/0000-0001-6310-9765

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 08 January 2020

Publication date Collection: 2020

Volume: 9

Electronic Location Identifier: e53832

Affiliations

[1]deptDepartment of Biomedical Science University of Sheffield SheffieldUnited Kingdom

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Daniel JE Green https://orcid.org/0000-0001-8282-6268

Andrew C Lin https://orcid.org/0000-0001-6310-9765

Article

Publisher ID: 53832

DOI: 10.7554/eLife.53832

PMC ID: 6949011

SO-VID: 51e5763e-81eb-488c-bda6-9560bca74312

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This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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Date received : 02 January 2020

Date accepted : 02 January 2020

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Author impact statement Some dopaminergic neurons release both dopamine and nitric oxide to increase the flexibility of olfactory memories.

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ScienceOpen disciplines: Life sciences

Keywords: associative learning,memory dynamics,dopamine,cotransmitter,nitric oxide,mushroom body,d. melanogaster

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ScienceOpen disciplines: Life sciences

Keywords: associative learning, memory dynamics, dopamine, cotransmitter, nitric oxide, mushroom body, d. melanogaster

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How nitric oxide helps update memories

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cGMP: Generators, Effectors and Therapeutic Implications Conference

Most cited references 4

Behavioral consequences of dopamine deficiency in the Drosophila central nervous system.

A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP.

Are mushroom bodies cerebellum-like structures?

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Cited by 1

Most referenced authors 73