Associative Learning and CA3–CA1 Synaptic Plasticity Are Impaired in D1R Null,Drd1a−/−Mice and in Hippocampal siRNA Silenced Drd1a Mice

Ortiz, Oskar; Delgado-García, José María; Espadas, Isabel; Bahí, Amine; Trullas, Ramón; Dreyer, Jean-Luc; Gruart, Agnès; Moratalla, Rosario

doi:10.1523/jneurosci.2655-10.2010

Cited by 143Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

Associative Learning and CA3–CA1 Synaptic Plasticity Are Impaired in D1R Null,Drd1a−/−Mice and in Hippocampal siRNA Silenced Drd1a Mice

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Ortiz, Oskar, Delgado-García, José María, Espadas, Isabel, Bahí, Amine, Trullas, Ramón, Dreyer, Jean-Luc, Gruart, Agnès, Moratalla, Rosario·2010·The Journal of Neuroscience

DOI 10.1523/jneurosci.2655-10.2010PMC PMC6633447

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Abstract

Associative learning depends on multiple cortical and subcortical structures, including striatum, hippocampus, and amygdala. Both glutamatergic and dopaminergic neurotransmitter systems have been implicated in learning and memory consolidation. While the role of glutamate is well established, the role of dopamine and its receptors in these processes is less clear. In this study, we used two models of dopamine D(1) receptor (D(1)R, Drd1a) loss, D(1)R knock-out mice (Drd1a(-/-)) and mice with intrahippocampal injections of Drd1a-siRNA (small interfering RNA), to study the role of D(1)R in different models of learning, hippocampal long-term potentiation (LTP) and associated gene expression. D(1)R loss markedly reduced spatial learning, fear learning, and classical conditioning of the eyelid response, as well as the associated activity-dependent synaptic plasticity in the hippocampal CA1-CA3 synapse. These results provide the first experimental demonstration that D(1)R is required for trace eyeblink conditioning and associated changes in synaptic strength in hippocampus of behaving mice. Drd1a-siRNA mice were indistinguishable from Drd1a(-/-) mice in all experiments, indicating that hippocampal knockdown was as effective as global inactivation and that the observed effects are caused by loss of D(1)R and not by indirect developmental effects of Drd1a(-/-). Finally, in vivo LTP and LTP-induced expression of Egr1 in the hippocampus were significantly reduced in Drd1a(-/-) and Drd1a-siRNA, indicating an important role for D(1)R in these processes. Our data reveal a functional relationship between acquisition of associative learning, increase in synaptic strength at the CA3-CA1 synapse, and Egr1 induction in the hippocampus by demonstrating that all three are dramatically impaired when D(1)R is eliminated or reduced.

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DA can influence the persistence of aversive learning.
“studies also have indicated that DA can influence the persistence of aversive learning (Moncada et al., 2011; Ortiz et al., 2010; Rossato et al., 2009).”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as Ortiz et al., 2010
Learning of responses to aversive stimuli in rodents during fear conditioning is inhibited by dopaminergic antagonists.
“learning of responses to aversive stimuli in rodents (ie. during fear conditioning) is inhibited by dopaminergic antagonists [66–68].”
From A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP (2011) · cites this paper as [67]

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Authors: Ortiz, O., Delgado-García, J. M., Espadas, I., Bahí, A., Trullas, R., Dreyer, J.-L., Gruart, A., & Moratalla, R.
Affiliations: Consejo Superior de Investigaciones Científicas (ES)
University of Fribourg (CH)
Universidad Pablo de Olavide (ES)
ORCID: Espadas, Isabel
Bahí, Amine
Dreyer, Jean-Luc
Gruart, Agnès
Moratalla, Rosario
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2010-09-15
Volume: 30
Issue: 37
Pages: 12288-12300
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.2655-10.2010
PMC: PMC6633447
OpenAlex: W1984592720
Cited by: 143
References: 79
Citations by year: 2026: 2 · 2025: 2 · 2024: 3 · 2023: 3 · 2022: 15 · 2021: 4 · 2020: 8 · 2019: 7 · 2018: 2 · 2017: 10 · 2016: 11 · 2015: 9 · 2014: 18 · 2013: 21 · 2012: 13
FWCI: 9.50
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 181 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
Funders: Eusko Jaurlaritza
Ministerio de Ciencia e Innovación (BFU2010-20664)
Plan Nacional sobre Drogas
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: dopamine D1 receptor, associative learning, hippocampal synaptic plasticity, CA3-CA1 synapses, long-term potentiation, EGR1, eyeblink conditioning, spatial learning, fear learning, siRNA knockdown, hippocampus
MeSH terms: Animals, Association Learning, Gene Expression Regulation, Hippocampus, Male, Mice, Inbred C57BL, Neural Inhibition, Synaptic Transmission, Neuronal Plasticity, Receptors, Dopamine D1, Long-Term Potentiation, Mice, Knockout, RNA Interference, RNA, Small Interfering, Mice, Early Growth Response Protein 1, CA1 Region, Hippocampal, CA3 Region, Hippocampal

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Associative Learning and CA3–CA1 Synaptic Plasticity Are Impaired in D1R Null,Drd1a−/−Mice and in Hippocampal siRNA Silenced Drd1a Mice

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