Evidence map›Paper›PMID 36130601›Full record

ArticleCurrent biology : CB2022

Lateral axonal modulation is required for stimulus-specific olfactory conditioning in Drosophila.

Julia E Manoim, Andrew M Davidson, Shirley Weiss, Toshihide Hige, Moshe Parnas

Abstract read
In one paragraph

Article in Current biology : CB, 2022. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 28 papers.

0numbers the graph read from it
0cells of the map it votes in
28citing papers in PubMed
–field-weighted citation impact
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

28 citing papers in PubMed.

  1. Article
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  8. The GABAiScience · 2025
    Article
  9. Article
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  14. Review
  15. Article
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  18. Article
  19. Use-Dependent, Untapped Dual Kinase Signaling Localized in Brain Learning Circuitry.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2024
    Article
  20. Article
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

5 authors.

Julia E ManoimDepartment of Physiology and Pharmacology, Sackler School of Medicine, Tel Aviv University, Tel Aviv 69978, Israel.
Andrew M DavidsonDepartment of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
Shirley WeissDepartment of Physiology and Pharmacology, Sackler School of Medicine, Tel Aviv University, Tel Aviv 69978, Israel.
Toshihide HigeDepartment of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA; Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA; Integrative Program for Biological and Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA. Electronic address: hige@email.unc.edu.
Moshe ParnasDepartment of Physiology and Pharmacology, Sackler School of Medicine, Tel Aviv University, Tel Aviv 69978, Israel; Sagol School of Neuroscience, Tel Aviv University, Tel Aviv 69978, Israel. Electronic address: mparnas@tauex.tau.ac.il.

Funding

Resource Component: Acquisition, maintenance and distribution of Drosophila stocksP40OD018537 · OD · TRUSTEES OF INDIANA UNIVERSITY · PI Annette L. Parks · 2014 to 2026
$13.5M
DROSOPHILA GENOMICS RESOURCE CENTERP40OD010949 · OD · TRUSTEES OF INDIANA UNIVERSITY · PI Andrew Zelhof · 2012 to 2026
$9.4M
Molecular and circuit mechanisms of learning supported by heterogeneous dopaminergic neuronsR01DC018874 · NIDCD · UNIV OF NORTH CAROLINA CHAPEL HILL · PI TOSHIHIDE HIGE · 2021 to 2026
$1.6M
The representation and modulation of sensory information in the learning and memory center of the Drosophila brainF32MH125582 · NIMH · UNIV OF NORTH CAROLINA CHAPEL HILL · PI DAVIDSON, ANDREW M · 2021 to 2023
$223k
NIDCD NIH HHS R01 DC018874NIH HHS P40 OD010949NIH HHS P40 OD018537NIMH NIH HHS F32 MH125582
6 · The paper itself

Abstract

Effective and stimulus-specific learning is essential for animals' survival. Two major mechanisms are known to aid stimulus specificity of associative learning. One is accurate stimulus-specific representations in neurons. The second is a limited effective temporal window for the reinforcing signals to induce neuromodulation after sensory stimuli. However, these mechanisms are often imperfect in preventing unspecific associations; different sensory stimuli can be represented by overlapping populations of neurons, and more importantly, the reinforcing signals alone can induce neuromodulation even without coincident sensory-evoked neuronal activity. Here, we report a crucial neuromodulatory mechanism that counteracts both limitations and is thereby essential for stimulus specificity of learning. In Drosophila, olfactory signals are sparsely represented by cholinergic Kenyon cells (KCs), which receive dopaminergic reinforcing input. We find that KCs have numerous axo-axonic connections mediated by the muscarinic type-B receptor (mAChR-B). By using functional imaging and optogenetic approaches, we show that these axo-axonic connections suppress both odor-evoked calcium responses and dopamine-evoked cAMP signals in neighboring KCs. Strikingly, behavior experiments demonstrate that mAChR-B knockdown in KCs impairs olfactory learning by inducing undesired changes to the valence of an odor that was not associated with the reinforcer. Thus, this local neuromodulation acts in concert with sparse sensory representations and global dopaminergic modulation to achieve effective and accurate memory formation.

Indexed as

DrosophilaMushroom BodiesAnimalsCalciumCholinergic AgentsDopamineDrosophila melanogasterOdorantsSmellCalciumCholinergic AgentsDopamineassociative learning and memoryaxo-axonal lateral neuromodulationaxonal modulationDrosophilaKenyon cellsmuscarinic receptorsmushroom bodynon-specific conditioning

Identifiers

PMID36130601
PMCPMC9613607

What OpenQuestion holds

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Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.