Parvalbumin tunes spike‐timing and efferent short‐term plasticity in striatal fast spiking interneurons
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Key points: Fast spiking interneurons (FSIs) modulate output of the striatum and are implicated in severe motor disorders. Selective expression of the calcium‐binding protein parvalbumin (PV) in FSIs raises questions about how PV controls FSI Ca 2+ dynamics. Here we report a novel mechanism linking PV‐Ca 2+ buffering and FSI spiking as a result of the activation of small conductance (SK) Ca 2+‐dependent K+ channels. We also show that, at the presynaptic terminals, PV prevents synaptic facilitation at narrow frequencies at FSI to striatal output neuron synapses. Our data establish that PV is a key element in providing rhythm generation in FSIs as well as filtering striatal output. Thus, FSI neuromodulation via PV and/or SK channels is an interesting target for controlling the establishment of oscillatory frequencies related to the induction or worsening of pathology‐related motor rhythms. Abstract Striatal fast spiking interneurons (FSIs) modulate output of the striatum by synchronizing medium‐sized spiny neurons (MSNs). Recent studies have broadened our understanding of FSIs, showing that they are implicated in severe motor disorders such as parkinsonism, dystonia and Tourette syndrome. FSIs are the only striatal neurons to express the calcium‐binding protein parvalbumin (PV). This selective expression of PV raises questions about the functional role of this Ca 2+ buffer in controlling FSI Ca 2+ dynamics and, consequently, FSI spiking mode and neurotransmission. To study the functional involvement of FSIs in striatal microcircuit activity and the role of PV in FSI function, we performed perforated patch recordings on enhanced green fluorescent protein‐expressing FSIs in brain slices from control and PV−/− mice. Our results revealed that PV−/− FSIs fired more regularly and were more excitable than control FSIs by a mechanism in which Ca 2+ buffering is linked to spiking activity as a result of the activation of small conductance Ca 2+‐dependent K+ channels. A modelling approach of striatal FSIs supports our experimental results. Furthermore, PV deletion modified frequency‐specific short‐term plasticity at inhibitory FSI to MSN synapses. Our results therefore reinforce the hypothesis that in FSIs, PV is crucial for fine‐tuning of the temporal responses of the FSI network and for the orchestration of MSN populations. This, in turn, may play a direct role in the generation and pathology‐related worsening of motor rhythms.
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Parvalbumin is important in short-term plasticity in striatal neurons, and loss of parvalbumin can affect the excitability and output of these cells.
“Furthermore, PV is important in short-term plasticity in striatal neurons and loss of PV can affect the excitability and output of these cells (Orduz et al, 2013).”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Orduz et al, 2013
In striatal PV+ FSI, the increased facilitation (increased inhibition) between FSI and medium spiny neurons (MSN) caused by the absence of PV in PV-/- mice is partly compensated by a decrease in the excitatory synaptic input from cortical pyramidal cells, a mechanism hypothesized to compensate for the increased output of PV-/- neurons.
“In striatal PV+ FSI the increased facilitation (increased inhibition) between FSI and medium spiny neurons (MSN) caused by the absence of PV in PV-/-mice [53] is partly compensated by a decrease in the excitatory synaptic input from cortical pyramidal cells, a mechanism hypothesized to compensate for the increased output of PV-/- neurons [48].”
The demonstration that PV levels are decreased may indicate a shift in the E/I balance towards increased inhibition, taking into account the proven role of PV in synaptic transmission.
“In addition, the demonstration that PV levels are decreased may indicate a shift in the E/I balance towards an increased inhibition, taking into account the proven role of PV in synaptic transmission [52, 53, 55, 97, 98].”
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- C 2013 The Authors. The Journal of Physiology C 2013 The Physiological Society 14697793, 2013, 13, J Physiol 591. · DOI
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- Authors
- Orduz, D., Bischop, D. P., Schwaller, B., Schiffmann, S. N., & Gall, D.
- Affiliations
- Université Libre de Bruxelles (BE)
- University of Fribourg (CH)
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2013-04-30
- Volume
- 591
- Issue
- 13
- Pages
- 3215-3232
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC3717224
- OpenAlex
- W2153738580
- Cited by
- 88
- References
- 64
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 13 · 2023: 2 · 2022: 6 · 2021: 8 · 2020: 8 · 2019: 5 · 2018: 8 · 2017: 5 · 2016: 9 · 2015: 7 · 2014: 7 · 2013: 2
- FWCI
- 4.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- Funders
- Fonds De La Recherche Scientifique - FNRS
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Keywords
- parvalbumin, fast-spiking interneurons, striatum, small conductance calcium-activated potassium channels, calcium buffering, spike timing, short-term plasticity, synaptic facilitation, medium spiny neurons, motor rhythm, neuromodulation, Parkinson's disease, dystonia
- MeSH terms
- Animals, Corpus Striatum, Interneurons, Mice, Inbred C57BL, Mice, Transgenic, Models, Biological, Neuronal Plasticity, Parvalbumins, Mice, In Vitro Techniques
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