Postsynaptic origin of CB1‐dependent tonic inhibition of GABA release at cholecystokinin‐positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus

Neu, Axel; Földy, Csaba; Soltész, Iván

doi:10.1113/jphysiol.2006.115691

Cited by 167 publications

(201 citation statements)

References 48 publications

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“…3) are thought to play complementary roles to FSBCs, because of their different input and output properties (Hefft and Jonas, 2005;Földy et al, 2006;Glickfeld and Scanziani, 2006), regulation by modulatory systems Freund and Katona, 2007;Neu et al, 2007) and in vivo firing properties (Klausberger et al, 2005). In our sample, all RSBCs had the majority of their axons arborizing in the pyramidal cell layer of CA3 (24 of 24; all cells), forming large, closely placed boutons.…”

Section: Specific Description Of Cell Typesmentioning

confidence: 96%

Functional Specificity of Mossy Fiber Innervation of GABAergic Cells in the Hippocampus

Szabadics¹,

Soltész²

2009

J. Neurosci.

105

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One million mossy fibers in the rat provide individually sparse but functionally important synaptic connections between the dentate gyrus and hippocampus. Although the majority of mossy fiber targets are GABAergic cells, the functional organization of the feedforward GABAergic machinery modulating the interactions of granule cells and CA3 pyramidal cells are not yet understood. We used mossy fiber bouton to GABA neuron paired recordings in the CA3 to demonstrate that mossy fibers provide cell type-specific innervation to distinct GABAergic neurons with specialized intra-and extrahippocampal outputs. Our results show that mossy fibers contact the perisomatically projecting fast-spiking and regular-spiking basket cells, in addition to the dendritically projecting ivy cells, and the septum-projecting spiny stratum lucidum cells. Monosynaptic mossy fiber inputs to fast-spiking basket cells and spiny stratum lucidum cells were found to be numerous, but they were small in amplitude and displayed low transmission probabilities. In contrast, regular-spiking basket cells and ivy cells were less likely to be innervated by mossy fibers, but the amplitudes of mossy fiber EPSCs were large and the transmission probabilities were high. The dependence of the numbers and strengths of the mossy fiber inputs to CA3 GABAergic cells on the postsynaptic cell type was correlated with the frequency of the background synaptic events, so that cells with weak but numerous mossy fiber inputs received high rates of spontaneous synaptic events. Together, these results reveal the diverse components and high degree of functional specificity of the GABAergic cellular machinery underlying the dentate gyrus-CA3 interface.

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Section: Specific Description Of Cell Typesmentioning

confidence: 96%

Functional Specificity of Mossy Fiber Innervation of GABAergic Cells in the Hippocampus

Szabadics¹,

Soltész²

2009

J. Neurosci.

105

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“…Tracing studies had established that CCK hippocampal interneurons receive cholinergic inputs from the septum (Woolf, 1991) and serotonergic afferents from the median raphe nucleus (Freund et al, 1990). In addition, electrophysiological analysis determined that the tonic control of GABA release from hippocampal CCK cells is regulated through the modulation of the synthesis and release of endocannabinoids from the postsynaptic pyramidal neurons (Kim et al, 2002;Neu et al, 2007). The complex composition of these α7 nACh/ 5HT3 A /CB1/CCK interneurons is in line with the suggestion that hippocampal CCK neurons relay inputs from diverse cortical and subcortical regions about emotional, motivational, and physiological states (Freund, 2003).…”

Section: Hippocampal α7 Nach/cb1/5ht3 a /Cck Interneuronsmentioning

confidence: 99%

“…In addition, we determined that, with exception of the s. oriens, in both the hippocampus and the DG the interneurons co-expressing α7 nACh mRNA and CB1 mRNA constitute the major population of CB1 containing interneurons. Based on the high degree of co-localization of α7 nACh mRNA and CB1 in these interneurons, it is likely that their GABAergic neurotransmission will be regulated by the synthesis and release of endocannabinoids from the postsynaptic pyramidal neurons (Kim et al, 2002;Neu et al, 2007) and by their cholinergic innervations from the medial septum and diagonal band (Woolf, 1991).Interneurons expressing α7 nACh mRNA constitute a subpopulation of CCK containing neurons in the hippocampus and the DGWe found that, with the exception of the s. oriens, in both the hippocampus and the DG 40-79% of all interneurons expressing α7 nACh mRNA contain CCK. In contrast, within the s. oriens only 20% of all interneurons expressing α7 nACh mRNA have CCK.…”

mentioning

confidence: 99%

Hippocampal interneurons co-express transcripts encoding the α7 nicotinic receptor subunit and the cannabinoid receptor 1

2008

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The notion of functional interactions between the α7 nicotinic acetylcholine (α7 nACh) and the cannabinoid systems is emerging from recent in vitro and in vivo studies. Both the α7 nACh receptor and the cannabinoid receptor 1 (CB1) are highly expressed in the hippocampus. To begin addressing possible anatomical interactions between the α7 nACh and the cannabinoid systems in the rat hippocampus, we investigated the distribution of neurons expressing α7 nACh mRNA in relation to those containing CB1 mRNA. By in situ hybridization we found that the α7 nACh mRNA is diffusely expressed in principal neurons and is highly expressed in a subset of interneurons. We observed that the pattern of distribution of hippocampal interneurons co-expressing transcripts encoding α7 nACh and glutamate decarboxylase (GAD; synthesizing enzyme of GABA) closely resembles the one displayed by interneurons expressing CB1 mRNA. By double in situ hybridization we established that the majority of hippocampal interneurons expressing α7 nACh mRNA have high levels of CB1 mRNA. As CB1 interneurons contain cholecystokinin (CCK), we investigated the degree of cellular co-expression of α7 nACh mRNA and CCK, and found that the cellular co-existence of α7 nACh and CCK varies within the different layers of the hippocampus.In summary, we established that most of the hippocampal α7 nACh expressing interneurons are endowed with CB1 mRNA. We found that these α7 nACh/CB1 interneurons are the major subpopulation of hippocampal interneurons expressing CB1 mRNA. The α7 nACh expressing interneurons represent half of the detected population of CCK containing neurons in the hippocampus. Since it is well established that the vast majority of hippocampal interneurons expressing CB1 mRNA have 5-HT type 3 (5-HT 3 ) receptors, we conclude that these hippocampal α7 nACh/5HT 3 /CB1/CCK interneurons correspond to those previously postulated to relay inputs from diverse cortical and subcortical regions about emotional, motivational, and physiological states. KeywordsCB1; 5-HT3 receptors; 5-HT; CCK; Alzheimer's disease; schizophrenia Nicotinic acetylcholine (nACh) receptors are members of the superfamily of ligand-gated ion channels that the includes the GABA receptors (GABA A and GABA C ), the glycine receptor and the 5-HT type 3 receptor (5-HT 3 R). In the nervous system, several subunits of the nACh receptor have been identified, including nine α subunits (α2-α10) and three β subunits (β2-β4) (Sargent, 1993;McGehee and Role, 1995 (Sargent, 1993;McGehee and Role, 1995). Electrophysiological, pharmacological and genetic approaches demonstrated that the homomeric α7-nACh receptor has a high affinity for α-bungarotoxin (Couturier et al., 1990;Séguéla et al., 1993;Chen and Patrick, 1997;Orr-Urtreger et al., 1997). The high affinity of the α7-nACh receptor for α-bungarotoxin has been used to map the distribution of this receptor in several brain areas, including the hippocampus (Hunt and Schmidt, 1978;Freedman et al., 1993;Fabian-Fine et al., 2001). Although mRNA enco...

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“…In the methods described above, pharmacological isolation and paired recordings are used to assess post and presynaptic GABA B R-mediated effects, respectively; however one can easily modify the combination of receptor agonists and antagonists to assess the role of alternative receptor families, for example the cannabinoid system 21 …”

Section: Discussionmentioning

confidence: 99%

Whole-cell Patch-clamp Recordings from Morphologically- and Neurochemically-identified Hippocampal Interneurons

Booker

Song

Vida

2014

JoVE

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GABAergic inhibitory interneurons play a central role within neuronal circuits of the brain. Interneurons comprise a small subset of the neuronal population (10-20%), but show a high level of physiological, morphological, and neurochemical heterogeneity, reflecting their diverse functions. Therefore, investigation of interneurons provides important insights into the organization principles and function of neuronal circuits. This, however, requires an integrated physiological and neuroanatomical approach for the selection and identification of individual interneuron types. Whole-cell patch-clamp recording from acute brain slices of transgenic animals, expressing fluorescent proteins under the promoters of interneuron-specific markers, provides an efficient method to target and electrophysiologically characterize intrinsic and synaptic properties of specific interneuron types. Combined with intracellular dye labeling, this approach can be extended with post-hoc morphological and immunocytochemical analysis, enabling systematic identification of recorded neurons. These methods can be tailored to suit a broad range of scientific questions regarding functional properties of diverse types of cortical neurons. Video LinkThe video component of this article can be found at

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Postsynaptic origin of CB1‐dependent tonic inhibition of GABA release at cholecystokinin‐positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus

Cited by 167 publications

References 48 publications

Functional Specificity of Mossy Fiber Innervation of GABAergic Cells in the Hippocampus

Functional Specificity of Mossy Fiber Innervation of GABAergic Cells in the Hippocampus

Hippocampal interneurons co-express transcripts encoding the α7 nicotinic receptor subunit and the cannabinoid receptor 1

Whole-cell Patch-clamp Recordings from Morphologically- and Neurochemically-identified Hippocampal Interneurons

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