GABAB Receptor Modulation of Feedforward Inhibition through Hippocampal Neurogliaform Cells
Open accessAbstract
Feedforward inhibition of neurons is a fundamental component of information flow control in the brain. We studied the roles played by neurogliaform cells (NGFCs) of stratum lacunosum moleculare of the hippocampus in providing feedforward inhibition to CA1 pyramidal cells. We recorded from synaptically coupled pairs of anatomically identified NGFCs and CA1 pyramidal cells and found that, strikingly, a single presynaptic action potential evoked a biphasic unitary IPSC (uIPSC), consisting of two distinct components mediated by GABA(A) and GABA(B) receptors. A GABA(B) receptor-mediated unitary response has not previously been observed in hippocampal excitatory neurons. The decay of the GABA(A) receptor-mediated response was slow (time constant = 50 ms), and was tightly regulated by presynaptic GABA(B) receptors. Surprisingly, the GABA(B) receptor ligands baclofen and (2S)-3-{[(1S)-1-(3,4-dichlorophenyl)ethyl]amino-2-hydroxypropyl}(phenylmethyl)phosphinic acid (CGP55845), while affecting the NGFC-mediated uIPSCs, had no effect on action potential-evoked presynaptic Ca2+ signals monitored in individual axonal boutons of NGFCs with two-photon microscopy. In contrast, baclofen clearly depressed presynaptic Ca2+ transients in non-NGF interneurons. Changes in extracellular Ca2+ concentration that mimicked the effects of baclofen or CGP55845 on uIPSCs significantly altered presynaptic Ca2+ transients. Electrophysiological data suggest that GABA(B) receptors expressed by NGFCs contribute to the dynamic control of the excitatory input to CA1 pyramidal neurons from the temporoammonic path. The NGFC-CA1 pyramidal cell connection therefore provides a unique and subtle mechanism to shape the integration time domain for signals arriving via a major excitatory input to CA1 pyramidal cells.
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The cloud of GABA generated from NGFC release can also activate presynaptic GABABR to mediate homosynaptic and heterosynaptic depression of GABAergic and glutamatergic release sometimes with remarkable target cell specificity.
“In addition, the cloud of GABA generated from NGFC release can also activate presynaptic GABABR to mediate homosynaptic and heterosynaptic depression of GABAergic and glutamatergic release (48, 858, 859, 926, 927) sometimes with remarkable target cell specificity (204).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [927]
NGFC dendrites and axons can also cross the hippocampal fissure into the molecular layer of the dentate gyrus and penetrate into superficial s.r., indicating that CA1 NGFC recruitment and distribution of inhibition extend beyond s.l.m.
“However, NGFC dendrites and axons can also cross the hippocampal fissure into the molecular layer of the dentate gyrus and penetrate into superficial s.r., indicating that CA1 NGFC recruitment and distribution of inhibition extend beyond s.l.m. (367, 550, 926, 927).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [927]
These features combined with the dense local ramification of NGFC axons are considered to underlie the ability of NGFCs to mediate volume transmission leading to slow dual component (GABAAR- and GABABR-mediated) inhibition at virtually any postsynaptic element within their dense axonal plexus.
“These features combined with the dense local ramification of NGFC axons are considered to underlie the ability of NGFCs to mediate volume transmission leading to slow dual component (GABAAR- and GABABR-mediated) inhibition at virtually any postsynaptic element within their dense axonal plexus (550, 926, 927, 1074, 1086).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [927]
NGFCs mediate postsynaptic GABABR-mediated responses on other NGFCs and principal cells even after a single action potential.
“It is evident that NGFCs mediate postsynaptic GABABR-mediated responses on other NGFCs and principal cells even after a single action potential (48, 927, 1086).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [927]
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“However, NGFCs are the only INs that have been shown so far to elicit robust unitary GABAB responses in response to a single AP (Tamás et al., 2003; Price et al., 2005, 2008; Wozny and Williams, 2011).”
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- Authors
- Price, C. J., Scott, R., Rusakov, D. A., & Capogna, M.
- Affiliations
- Medical Research Council (GB)
- UCL Queen Square Institute of Neurology (GB)
- Queen's University (CA)
- Aarhus University (DK)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2008-07-02
- Volume
- 28
- Issue
- 27
- Pages
- 6974-6982
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2685170
- OpenAlex
- W2036270719
- Cited by
- 107
- References
- 66
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 6 · 2023: 7 · 2022: 3 · 2021: 6 · 2020: 9 · 2019: 6 · 2018: 8 · 2017: 6 · 2016: 4 · 2015: 3 · 2014: 3 · 2013: 1 · 2012: 10
- FWCI
- 3.42
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Wellcome Trust (084311, 77987, 071179)
- European Commission
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- GABAB receptors, feedforward inhibition, neurogliaform cells, hippocampus, CA1 pyramidal neurons, presynaptic inhibition, baclofen, CGP55845, extracellular calcium, temporoammonic pathway, stratum lacunosum-moleculare, inhibitory interneurons
- MeSH terms
- Action Potentials, Animals, Baclofen, Calcium, gamma-Aminobutyric Acid, Hippocampus, Interneurons, Neural Inhibition, Neural Pathways, Synaptic Transmission, Neuroglia, Organ Culture Techniques, Phosphinic Acids, Propanolamines, Receptors, GABA-A, Pyramidal Cells, Receptors, GABA-B, GABA Agonists, GABA Antagonists, Calcium Signaling, Rats, Inhibitory Postsynaptic Potentials
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