Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning
Abstract
Learning and memory processes can be influenced by recent experience, but the mechanisms involved are poorly understood. Enhanced plasticity during critical periods of early life is linked to differentiating parvalbumin (PV)-interneuron networks, suggesting that recent experience may modulate learning by targeting the differentiation state of PV neurons in the adult. Here we show that environmental enrichment and Pavlovian contextual fear conditioning induce opposite, sustained and reversible hippocampal PV-network configurations in adult mice. Specifically, enrichment promotes the emergence of large fractions of low-differentiation (low PV and GAD67 expression) basket cells with low excitatory-to-inhibitory synaptic-density ratios, whereas fear conditioning leads to large fractions of high-differentiation (high PV and GAD67 expression) basket cells with high excitatory-to-inhibitory synaptic-density ratios. Pharmacogenetic inhibition or activation of PV neurons was sufficient to induce such opposite low-PV-network or high-PV-network configurations, respectively. The low-PV-network configuration enhanced structural synaptic plasticity, and memory consolidation and retrieval, whereas these were reduced by the high-PV-network configuration. We then show that maze navigation learning induces a hippocampal low-PV-network configuration paralleled by enhanced memory and structural synaptic plasticity throughout training, followed by a shift to a high-PV-network configuration after learning completion. The shift to a low-PV-network configuration specifically involved increased vasoactive intestinal polypeptide (VIP)-positive GABAergic boutons and synaptic transmission onto PV neurons. Closely comparable low- and high-PV-network configurations involving VIP boutons were specifically induced in primary motor cortex upon rotarod motor learning. These results uncover a network plasticity mechanism induced after learning through VIP-PV microcircuit modulation, and involving large, sustained and reversible shifts in the configuration of PV basket-cell networks in the adult. This novel form of experience-related plasticity in the adult modulates memory consolidation, retrieval and learning, and might be harnessed for therapeutic strategies to promote cognitive enhancement and neuroprotection.
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ODP may be promoted by reducing parvalbumin-expressing interneuron activity in bV1.
“ODP may be promoted by reducing parvalbumin-expressing (PVs) interneuron activity in bV1 (Caillard et al., 2000;Donato et al., 2013;Reh et al., 2020).”
From Psychedelics and Neural Plasticity: Therapeutic Implications (2022) · cites this paper as Donato et al., 2013
In the perirhinal cortex and hippocampus, ChABC digestion increases inhibitory inputs to PV interneurons.
“In the perirhinal cortex and hippocampus, ChABC digestion increases inhibitory inputs to PV interneurons [43–45]”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [43]
High PV expression hippocampal PV1 cells receive less inhibition and more excitation inputs than low PV expression cells in their dendritic compartment.
“A previous report, focused on hippocampal PV1 cells, described that high PV expression cells receive less inhibition and more excitation inputs than low PV expression cells, but in their dendritic compartment (Donato et al., 2013).”
From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Donato et al., 2013
The expression level of PV can be used to classify PV1 cells into different subpopulations regarding their activity and connectivity patterns.
“the expression level of PV can be used to classify them in different subpopulations regarding their activity and connectivity patterns”
From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Donato et al., 2013
Dendritic inhibition may be decreased in high PV expression cells and may be more sensitive to stimuli such as environmental enrichment.
“By contrast, dendritic inhibition may be decreased in these cells and may be more sensitive to stimuli, such as environmental enrichment (Donato et al., 2013).”
From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Donato et al., 2013
Reduced PV and CB1 expression may indicate a reduced activity level in PV cells and an altered endocannabinoid tone.
“This may indicate a reduced activity level in PV cells (Donato et al., 2013;Caballero et al., 2014) and an altered endocannabinoid tone”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Donato et al., 2013
GAD67 expression is highly sensitive to input and network activity and directly impacts magnitude of GABAergic transmission.
“As a rate-limiting GABA synthetic enzyme, GAD67 expression is highly sensitive to input and network activity and directly impacts the magnitude GABAergic transmission (43,48).”
From MeCP2 regulates the timing of critical period plasticity that shapes functional connectivity in primary visual cortex (2015) · cites this paper as [48]
PV-IN networks are associated with plasticity from early life through adulthood.
“These networks are associated with plasticity from early life throughout adulthood [70][71][72][73].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [70]
PV+ basket cells dynamically oscillate between different states in response to neuronal activity, a process required for learning and memory in the adult brain.
“For example, PV+ basket cells seem to dynamically oscillate between different “states” in response to neuronal activity, a process that is required for learning and memory in the adult brain (Donato et al., 2013; Lagler et al., 2016).”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Donato et al., 2013
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- Authors
- Donato, F., Rompani, S. B., & Caroni, P.
- Affiliations
- Friedrich Miescher Institute (CH)
- Corresponding author
- Caroni, Pico
- Venue
- Nature
- Published
- 2013-12-11
- Volume
- 504
- Issue
- 7479
- Pages
- 272-276
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2025806474
- Cited by
- 703
- References
- 4
- Citations by year
- 2026: 36 · 2025: 54 · 2024: 49 · 2023: 57 · 2022: 54 · 2021: 62 · 2020: 73 · 2019: 56 · 2018: 64 · 2017: 65 · 2016: 51 · 2015: 42 · 2014: 39 · 2013: 1
- FWCI
- 24.22
- Type
- journal article
- Language
- en
- Update notices
- correction (2025-05-02)
- Open access
- closed
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- edoc (University of Basel) (submittedVersion)
- Funders
- Novartis Foundation
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- parvalbumin, basket cells, interneurons, hippocampus, adult learning, synaptic plasticity, environmental enrichment, fear conditioning, GAD67, memory consolidation, memory retrieval, network configuration, cognitive enhancement, neuroprotection, critical period, trial-and-error learning, memory reconsolidation
- MeSH terms
- Animals, Cell Differentiation, Conditioning, Classical, Fear, Glutamate Decarboxylase, Hippocampus, Interneurons, Learning, Male, Memory, Synaptic Transmission, Neuronal Plasticity, Parvalbumins, Vasoactive Intestinal Peptide, Maze Learning, Biomedical Enhancement, Mice, GABAergic Neurons
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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