Evidence map›Paper›PMID 32360730›Full record

ArticleNeurobiology of learning and memory2020

Repeating or spacing learning sessions are strategies for memory improvement with shared molecular and neuronal components.

Verónica Cattaneo, Alvaro San Martin, Sergio E Lew, Bruce D Gelb, Mario R Pagani

Open access · bronzeAbstract read
In one paragraph

Article in Neurobiology of learning and memory, 2020. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 5 papers.

0numbers the graph read from it
0cells of the map it votes in
5citing papers in PubMed
0.2field-weighted citation impact, top 51% of its field
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

5 citing papers in PubMed, 4 citations in OpenAlex.

  1. The pERKs of temporal order memory in mice.Frontiers in molecular neuroscience · 2026
    Article
  2. Neurofibromin Deficiency Alters the Patterning and Prioritization of Motor Behaviors in a State-Dependent Manner.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2025
    Article
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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 at 3 institutions in 2 countries.

Verónica CattaneoIFIBIO-Houssay, Grupo de Neurociencia de Sistemas, Facultad de Medicina, Universidad de Buenos Aires - CONICET, 2155 Paraguay Street, Buenos Aires, Argentina.
Alvaro San MartinIFIBIO-Houssay, Grupo de Neurociencia de Sistemas, Facultad de Medicina, Universidad de Buenos Aires - CONICET, 2155 Paraguay Street, Buenos Aires, Argentina.
Sergio E LewInstituto de Ingeniería Biomédica, Facultad de Ingeniería, Universidad de Buenos Aires, Argentina.
Bruce D GelbMindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
Mario R PaganiIFIBIO-Houssay, Grupo de Neurociencia de Sistemas, Facultad de Medicina, Universidad de Buenos Aires - CONICET, 2155 Paraguay Street, Buenos Aires, Argentina. Electronic address: pagani@fmed.uba.ar.
University of Buenos Aires · ARChild Health and Development Institute · USConsejo Nacional de Investigaciones Científicas y Técnicas · AR

Funding

Pediatric Heart Disease: Getting from Mutations to TherapeuticsR35HL135742 · NHLBI · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI GELB, BRUCE D · 2017 to 2023
$6.1M
Understanding intellectual disability in Noonan syndrome and related disordersR03TW009010 · FIC · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI GELB, BRUCE D · 2011 to 2013
$158k
FIC NIH HHS R03 TW009010NHLBI NIH HHS R35 HL135742
6 · The paper itself

Abstract

Intellectual disability is a common feature in genetic disorders with enhanced RAS-ERK1/2 signaling, including neurofibromatosis type 1 (NF1) and Noonan syndrome (NS). Additional training trials and additional spacing between trials, respectively, restores memory deficits in animal models of NF1 and NS. However, the relationship between the underlying mechanisms in these strategies remain obscure. Here, we developed an approach to examine the effect of adding training trials or spacing to a weak training protocol and used genetic and behavioral manipulations in Drosophila to explore such question. We found that repetition and spacing effects are highly related, being equally effective to improve memory in control flies and sharing mechanistic bases, including the requirement of RAS activity in mushroom body neurons and protein synthesis dependence. After spacing or repeating learning trials, memory improvement depends on the formation of long-term memory (LTM). Moreover, a disease-related gain-of-function RasV152G allele impaired LTM. Using minimal training protocols, we established that both learning strategies were also equally effective for memory rescue in the RasV152G mutant and showed non-additive interaction of the spacing and repetition effects. Memory improvement was never detected after Ras inhibition. We conclude that memory improvement by spacing or repeating training trials are two ways of using the same molecular resources, including RAS-ERK1/2-dependent signaling. This evidence supports the concept that learning problems in RAS-related disorders depend on the impaired ability to exploit the repetition and the spacing effect required for long-term memory induction.

Indexed as

MAP Kinase Signaling SystemAnimalsBehavior, AnimalDrosophilaDrosophila ProteinsLearningMemory, Long-TermMushroom BodiesNeuronsras ProteinsDrosophila Proteinsras ProteinsDrosophilaMemory improvement strategiesMemory rescueRASopathies

Identifiers

PMID32360730
PMCPMC7451235
OpenAlexW3021020282

What OpenQuestion holds

Textmetadata
LicenceTDM
Read underepoch 390

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.