Regulation of cortical microcircuits by unitary GABA-mediated volume transmission
Open accessAbstract
GABA (gamma-aminobutyric acid) is predominantly released by local interneurons in the cerebral cortex to particular subcellular domains of the target cells. This suggests that compartmentalized, synapse-specific action of GABA is required in cortical networks for phasic inhibition. However, GABA released at the synaptic cleft diffuses to receptors outside the postsynaptic density and thus tonically activates extrasynaptic GABA(A) and GABA(B) receptors, which include subtypes of both receptor families especially sensitive to low concentrations of GABA. The synaptic and extrasynaptic action of GABA corroborates the idea that neurons of the brain use synaptic (or wiring) transmission and non-synaptic (or volume) transmission for communication. However, re-uptake mechanisms restrict the spatial extent of extrasynaptic GABA-mediated effects, and it has been proposed that the concerted action of several presynaptic interneurons, the sustained firing of individual cells or an increase in release-site density is required to reach ambient GABA levels sufficient to activate extrasynaptic receptors. Here we show that individual neurogliaform cells release enough GABA for volume transmission within the axonal cloud and, thus, that neurogliaform cells do not require synapses to produce inhibitory responses in the overwhelming majority of nearby neurons. Neurogliaform cells suppress connections between other neurons acting on presynaptic terminals that do not receive synapses at all in the cerebral cortex. They also reach extrasynaptic, delta-subunit-containing GABA(A) (GABA(Adelta)) receptors responsible for tonic inhibition. We show that GABA(Adelta) receptors are localized to neurogliaform cells preferentially among cortical interneurons. Neurosteroids, which are modulators of GABA(Adelta) receptors, alter unitary GABA-mediated effects between neurogliaform cells. In contrast to the specifically placed synapses formed by other interneurons, the output of neurosteroid-sensitive neurogliaform cells represents the ultimate form of the lack of spatial specificity in GABA-mediated systems, leading to long-lasting network hyperpolarization combined with widespread suppression of communication in the local circuit.
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An unusual anatomical feature of NGFCs is their remarkably high density of small area en passant boutons that in many cases (50-75% of terminals) do not have clear postsynaptic targets.
“An unusual anatomical feature of NGFCs is their remarkably high density of small area en passant boutons that in many cases (50–75% of terminals) do not have clear postsynaptic targets (102, 858, 1172).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
Molecular markers associated with NGFCs include NPY, reelin, neuronal nitric oxide synthase (nNOS), α-actinin 2, and COUP transcription factor 2 (COUPTF2).
“Molecular markers associated with NGFCs include NPY, reelin, neuronal nitric oxide synthase (nNOS), α-actinin 2, and COUP transcription factor 2 (COUPTF2) (48, 367, 549, 796, 858, 926, 1137).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
Even at synaptic junctions with identifiable postsynaptic elements (typically principal cell spines, spine necks, or dendritic shafts), NGFC inputs exhibit a strikingly wide synaptic cleft.
“Even at synaptic junctions with identifiable postsynaptic elements (typically principal cell spines, spine necks, or dendritic shafts), NGFC inputs exhibit a strikingly wide synaptic cleft (858).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
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 [858]
While neocortical NGFCs can be found throughout all layers, they are particularly enriched in supragranular layers and form a major constituent cell population in L1.
“While neocortical NGFCs can be found throughout all layers, they are particularly enriched in supragranular layers and form a major constituent cell population in L1 (564, 858, 1017, 1074, 1086, 1134).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
The bouton density of a single NGFC matches the release site density of five or six overlapping basket cell axons.
“Indeed, the bouton density of a single NGFC matches the release site density of five or six 6 overlapping basket cell axons (858).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
In contrast to the rapid and synchronous IPSCs produced by PVBCs, transmission from NGFCs generates long-lasting IPSCs resulting from prolonged GABA transients that arise from the unusual synaptic architecture where bouton density is high but close apposition to specialized postsynaptic densities is low.
“Of particular interest, in contrast to the rapid and synchronous IPSCs produced by PVBCs, transmission from NGFCs generates long-lasting IPSCs resulting from prolonged GABA transients (550, 1074, 1086) that arise from the unusual synaptic architecture where bouton density is high but close apposition to specialized postsynaptic densities is low (550, 751, 858, 1074) (FIGURE 13C).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
The vast majority of NGFC presynaptic boutons are spatially located at a larger than usual distance from their target dendrites and are often not in register with any clear postsynaptic structure.
“One feature of NGFC axons separating them from all other inhibitory interneurons is that the vast majority of presynaptic boutons are spatially located at a larger than usual distance from their target dendrites and are often not in register with any clear postsynaptic structure (858, 870).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
In somatosensory cortex, the separation between NGFC boutons and their dendrite targets averages 2.7 μm (range 1.1-5.0 μm).
“In somatosensory cortex, the separation between NGFC boutons and their dendrite targets averages 2.7 μm (range 1.1–5.0 μm) (858).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
The δ subunit is particularly abundant in PV interneurons and NGFCs with little or no detectable levels observed in SST-, CB-, or CR-expressing subtypes.
“The δ subunit is particularly abundant in PV interneurons (320, 788, 1256) and NGFCs (316, 858) with little or no detectable levels observed in SST-, CB-, or CR-expressing subtypes (788).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
THDOC-mediated effects are seen in interneuron subtypes expressing δ such as NGFCs and PV interneurons with little or no effect in SST cells that are devoid of this subunit.
“Thus THDOC-mediated effects are seen in interneuron subtypes expressing δ such as NGFCs and PV interneurons (316, 320, 788, 858, 1256) with little or no effect in SST cells that are devoid of this subunit (1160).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
Volume transmission by NGFCs also results in presynaptic GABABR activation on axon terminals of both PCs and other interneurons in a paracrine manner to modulate neurotransmitter release in cortical circuits.
“Volume transmission by NGFCs also results in presynaptic GABABR activation on axon terminals of both PCs and other interneurons in a paracrine manner to modulate neurotransmitter release in cortical circuits (204, 858).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [858]
Other mouse neocortical neurogliaform (Lamp5+) cell types are preferentially in upper layers and signal by volume transmission, diffuse GABA release without conventional synapses.
“Other neurogliaform (Lamp5+) cell types in the mouse neocortex are preferentially found in upper layers and signal by volume transmission, the diffuse release of the inhibitory neurotransmitter GABA in the absence of conventional synapses47.”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [47]
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Oxytocin Influences Male Sexual Activity via Non-synaptic Axonal Release in the Spinal Cord
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GABA Transporter GAT1: A Crucial Determinant of GABAB Receptor Activation in Cortical Circuits?
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- Authors
- Oláh, S., Füle, M., Komlósi, G., Varga, C., Báldi, R., Barzó, P., & Tamás, G.
- Affiliations
- University of Szeged (HU)
- Corresponding author
- Tamás, Gábor
- Venue
- Nature
- Published
- 2009-10
- Volume
- 461
- Issue
- 7268
- Pages
- 1278-1281
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2771344
- OpenAlex
- W2061619540
- Cited by
- 386
- References
- 32
- Citations by year
- 2026: 13 · 2025: 20 · 2024: 17 · 2023: 13 · 2022: 18 · 2021: 16 · 2020: 28 · 2019: 11 · 2018: 19 · 2017: 23 · 2016: 22 · 2015: 20 · 2014: 35 · 2013: 35 · 2012: 33
- FWCI
- 13.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Boehringer Ingelheim Fonds
- Magyar Tudományos Akadémia
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (NS535915, R01NS035915)
- 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 › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- neurogliaform cells, cortical microcircuits, neurosteroids, GABA reuptake, extrasynaptic GABAA receptors, postpartum depression, premenstrual syndrome, presynaptic inhibition
- MeSH terms
- Animals, Axons, gamma-Aminobutyric Acid, Interneurons, Models, Neurological, Neuroglia, Receptors, GABA-A, Somatosensory Cortex, Synapses, Rats, Wistar, Receptors, GABA-B, Paracrine Communication, Rats
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