Cholecystokinin-immunopositive basket and Schaffer collateral-associated interneurones target different domains of pyramidal cells in the CA1 area of the rat hippocampus

Cope, David W.; Maccaferri, Gianmaria; Márton, Lőrinc; Roberts, J. D. B.; Cobden, Philip M.; Somogyi, Péter

doi:10.1016/s0306-4522(01)00440-7

Cited by 130 publications

(147 citation statements)

References 114 publications

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“…Furthermore, as mentioned above, not every CCKϩ IN were mute in the CA3 area (Fig. 1b), indicating that CCKϩ INs are heterogeneous with respect to their initial P r and short-term plasticity, just as they are according to their input-output relationships and axodendritic arborizations [e.g., basket cells (1, 21), Schaffer collateralassociated INs (22), and MFA INs (12,20)]. …”

Section: Resultsmentioning

confidence: 83%

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Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons

Losonczy

Biró

Nusser

2004

Proc. Natl. Acad. Sci. U.S.A.

148

137

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Cortical information processing requires an orchestrated interaction between a large number of pyramidal cells and albeit fewer, but highly diverse GABAergic interneurons (INs). The diversity of INs is thought to reflect functional and structural specializations evolved to control distinct network operations. Consequently, specific cortical functions may be selectively modified by altering the input-output relationship of unique IN populations. Here, we report that persistently active cannabinoid receptors, the site of action of endocannabinoids, and the psychostimulants marijuana and hashish, switch off the output (mute) of a unique class of hippocampal INs. In paired recordings between cholecystokininimmunopositive, mossy fiber-associated INs, and their target CA3 pyramidal cells, no postsynaptic currents could be evoked with single presynaptic action potentials or with repetitive stimulations at frequencies <25 Hz. Cannabinoid receptor antagonists converted these ''mute'' synapses into high-fidelity ones. The selective muting of specific GABAergic INs, achieved by persistent presynaptic cannabinoid receptor activation, provides a state-dependent switch in cortical networks.hippocampus ͉ inhibition ͉ patch-clamp I nformation processing in the hippocampal neuronal network relies on precise, spatiotemporal reciprocal interactions between apparently homogeneous pyramidal cells (PCs) and highly diverse GABAergic interneurons (INs) (1-5). The impact of these nerve cells on their postsynaptic target cells is determined by a variety of factors, including the number and location of synapses on the postsynaptic cell, quantal size, probability of transmitter release (P r ), and short-or long-term synaptic plasticity (6). Many of these factors are highly variable at hippocampal glutamatergic synapses (7,8), despite the apparent uniformity of PCs. In contrast, at GABAergic synapses formed by the extremely diverse INs, many of these critical synaptic parameters seem to be alike. For example, hippocampal INs elicit postsynaptic responses that are highly reliable, of large amplitude, and predominantly show short-term depression (9-15). This type of synaptic transmission may be essential for INs synchronizing a large population of PCs (16). However, variability of these synaptic properties has been suggested to be beneficial for stabilizing the network (17). Furthermore, INs also convey autonomic, motivational, and emotional impact on hippocampal information processing, and this type of inhibition is supposed to be easily modifiable (18). In this article, we tested whether all GABAergic synaptic connections in the rat hippocampus were indeed highly reliable with apparent lack of transmission failures; or whether the output of an IN could be dramatically altered, implying a switch in their contribution to network behaviors. MethodsSlice Preparation and Electrophysiological Recordings. Horizontal hippocampal slices were prepared from 13-to 19-day-old male Wistar rats (15.9 Ϯ 0.3 days, n ϭ 26) as described earlier (19). After 1....

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Section: Resultsmentioning

confidence: 83%

“…CCK-immunopositive INs of the hippocampus include CCK͞vasoactive intestinal polypeptide- positive basket cells (1,21), CCKϩ Schaffer collateralassociated INs (22), and MFA INs. The presence of large amplitude, reliable postsynaptic responses in PCs on the activation of CCKϩ basket cells (Fig.…”

Section: Discussionmentioning

confidence: 99%

Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons

Losonczy

Biró

Nusser

2004

Proc. Natl. Acad. Sci. U.S.A.

148

137

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“…Scale bar ϭ 100 m in I (applies to A-I). (Harris et al, 1985;Nunzi et al, 1985), Schaffercollateral-associated interneurons (Vida et al, 1998;Cope et al, 2002), and the lacunosum-moleculare-perforant path-associated cells (Somogyi and Klausberger, 2005).…”

Section: ␤2ar Expression Predominates In Cholecystokinin-containing Imentioning

confidence: 99%

β‐adrenergic receptors are differentially expressed in distinct interneuron subtypes in the rat hippocampus

Cox

Racca

LeBeau

2008

J of Comparative Neurology

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Noradrenaline (NA) acting via ␤-adrenergic receptors (␤ARs) plays an important role in the modulation of memory in the hippocampus. ␤ARs have been shown to be expressed in principal cells, but their distribution across different interneuron classes is unknown. We have used specific interneuron markers including calcium binding proteins (parvalbumin, calbindin, and calretinin) and neuropeptides (somatostatin, neuropeptide Y, and cholecystokinin) together with either ␤1AR or ␤2AR to determine the distribution of these receptors in all major subfields of the hippocampus. We found that ␤1AR-expressing interneurons were more prevalent in the CA3 and CA1 regions of the hippocampus than in the dentate gyrus, where they were relatively sparse. ␤2AR-expressing interneurons were more uniformly distributed between all three regions of the hippocampus. A high proportion of neuropeptide Y-containing interneurons in the dentate gyrus co-expressed ␤2AR. ␤1AR labeling was common in interneurons expressing somatostatin and parvalbumin in the CA3 and CA1 regions, particularly in the stratum oriens of these regions. ␤2AR labeling was more likely to be found than ␤1AR labeling in cholecystokinin-expressing interneurons. In contrast, calretinin-containing interneurons were virtually devoid of ␤1AR or ␤2AR labeling. These regional and interneuron type-specific differences suggest functionally distinct roles for NA in modulating hippocampal activity via activation of ␤ARs.

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“…A few other mGluR8-decorated cells contained CR and may be IS (Freund and Buzsaki, 1996;Ferraguti et al, 2004). The rare calbindin-or CCK-positive neurons innervated by mGluR8 terminals may belong to the Schaffer collateral-associated interneurons expressing both CCK and calbindin (Cope et al, 2002). The unambiguous identification of these cells awaits visualization of their axonal patterns.…”

Section: Selective Expression Of Mglur8 In Relation To Specific Cell mentioning

confidence: 99%

Metabotropic Glutamate Receptor 8-Expressing Nerve Terminals Target Subsets of GABAergic Neurons in the Hippocampus

Ferraguti¹,

Klausberger²,

Cobden³

et al. 2005

J. Neurosci.

121

138

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Presynaptic metabotropic glutamate receptors (mGluRs) show a highly selective expression and subcellular location in nerve terminals modulating neurotransmitter release. We have demonstrated that alternatively spliced variants of mGluR8, mGluR8a and mGluR8b, have an overlapping distribution in the hippocampus, and besides perforant path terminals, they are expressed in the presynaptic active zone of boutons making synapses selectively with several types of GABAergic interneurons, primarily in the stratum oriens. Boutons labeled for mGluR8 formed either type I or type II synapses, and the latter were GABAergic. Some mGluR8-positive boutons also expressed mGluR7 or vasoactive intestinal polypeptide. Interneurons strongly immunopositive for the muscarinic M2 or the mGlu1 receptors were the primary targets of mGluR8-containing terminals in the stratum oriens, but only neurochemically distinct subsets were innervated by mGluR8-enriched terminals. The majority of M2-positive neurons were mGluR8 innervated, but a minority, which expresses somatostatin, was not. Rare neurons coexpressing calretinin and M2 were consistently targeted by mGluR8-positive boutons. In vivo recording and labeling of an mGluR8-decorated and strongly M2-positive interneuron revealed a trilaminar cell with complex spike bursts during theta oscillations and strong discharge during sharp wave/ripple events. The trilaminar cell had a large projection from the CA1 area to the subiculum and a preferential innervation of interneurons in the CA1 area in addition to pyramidal cell somata and dendrites. The postsynaptic interneuron type-specific expression of the high-efficacy presynaptic mGluR8 in both putative glutamatergic and in identified GABAergic terminals predicts a role in adjusting the activity of interneurons depending on the level of network activity.

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Cholecystokinin-immunopositive basket and Schaffer collateral-associated interneurones target different domains of pyramidal cells in the CA1 area of the rat hippocampus

Cited by 130 publications

References 114 publications

Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons

Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons

β‐adrenergic receptors are differentially expressed in distinct interneuron subtypes in the rat hippocampus

Metabotropic Glutamate Receptor 8-Expressing Nerve Terminals Target Subsets of GABAergic Neurons in the Hippocampus

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