Cell-type-specific modulation of feedback inhibition by serotonin in the hippocampus

Jochen Winterer; A Vanessa Stempel; Tamar Dugladze; Csaba Földy; Nino Maziashvili; Aleksandar R Zivkovic; Josef Priller; Ivan Soltesz; Tengis Gloveli; Dietmar Schmitz

doi:10.1523/JNEUROSCI.6382-10.2011

Cell-type-specific modulation of feedback inhibition by serotonin in the hippocampus

Jochen Winterer, A Vanessa Stempel, Tamar Dugladze, Csaba Földy, Nino Maziashvili, Aleksandar R Zivkovic, Josef Priller, Ivan Soltesz, Tengis Gloveli, Dietmar Schmitz

Research output: Contribution to journal › Article › peer-review

Abstract

Midbrain raphe nuclei provide strong serotonergic projections to the hippocampus, in which serotonin (5-HT) exerts differential effects mediated by multiple 5-HT receptor subtypes. The functional relevance of this diversity of information processing is poorly understood. Here we show that serotonin via 5-HT(1B) heteroreceptors substantially reduces synaptic excitation of cholecystokinin-expressing interneurons in area CA1 of the rat hippocampus, in contrast to parvalbumin-expressing basket cells. The reduction is input specific, affecting only glutamatergic synaptic transmission originating from CA1 pyramidal cells. As a result, serotonin selectively decreases feedback inhibition via 5-HT(1B) receptor activation and subsequently increases the integration time window for spike generation in CA1 pyramidal cells. Our data imply an important role for serotonergic modulation of GABAergic action in subcortical control of hippocampal output.

Original language	English
Pages (from-to)	8464-75
Number of pages	12
Journal	Journal of Neuroscience
Volume	31
Issue number	23
DOIs	https://doi.org/10.1523/JNEUROSCI.6382-10.2011
Publication status	Published - 8 Jun 2011

Keywords / Materials (for Non-textual outputs)

Animals
Cholecystokinin
Feedback, Physiological
Female
Glutamic Acid
Hippocampus
Immunohistochemistry
Male
Neural Inhibition
Neural Pathways
Neurons
Patch-Clamp Techniques
Raphe Nuclei
Rats
Rats, Wistar
Serotonin
Synaptic Transmission
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

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10.1523/JNEUROSCI.6382-10.2011

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title = "Cell-type-specific modulation of feedback inhibition by serotonin in the hippocampus",

abstract = "Midbrain raphe nuclei provide strong serotonergic projections to the hippocampus, in which serotonin (5-HT) exerts differential effects mediated by multiple 5-HT receptor subtypes. The functional relevance of this diversity of information processing is poorly understood. Here we show that serotonin via 5-HT(1B) heteroreceptors substantially reduces synaptic excitation of cholecystokinin-expressing interneurons in area CA1 of the rat hippocampus, in contrast to parvalbumin-expressing basket cells. The reduction is input specific, affecting only glutamatergic synaptic transmission originating from CA1 pyramidal cells. As a result, serotonin selectively decreases feedback inhibition via 5-HT(1B) receptor activation and subsequently increases the integration time window for spike generation in CA1 pyramidal cells. Our data imply an important role for serotonergic modulation of GABAergic action in subcortical control of hippocampal output.",

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author = "Jochen Winterer and Stempel, {A Vanessa} and Tamar Dugladze and Csaba F{\"o}ldy and Nino Maziashvili and Zivkovic, {Aleksandar R} and Josef Priller and Ivan Soltesz and Tengis Gloveli and Dietmar Schmitz",

year = "2011",

month = jun,

day = "8",

doi = "10.1523/JNEUROSCI.6382-10.2011",

language = "English",

volume = "31",

pages = "8464--75",

journal = "Journal of Neuroscience",

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publisher = "SOC NEUROSCIENCE",

number = "23",

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TY - JOUR

T1 - Cell-type-specific modulation of feedback inhibition by serotonin in the hippocampus

AU - Winterer, Jochen

AU - Stempel, A Vanessa

AU - Dugladze, Tamar

AU - Földy, Csaba

AU - Maziashvili, Nino

AU - Zivkovic, Aleksandar R

AU - Priller, Josef

AU - Soltesz, Ivan

AU - Gloveli, Tengis

AU - Schmitz, Dietmar

PY - 2011/6/8

Y1 - 2011/6/8

N2 - Midbrain raphe nuclei provide strong serotonergic projections to the hippocampus, in which serotonin (5-HT) exerts differential effects mediated by multiple 5-HT receptor subtypes. The functional relevance of this diversity of information processing is poorly understood. Here we show that serotonin via 5-HT(1B) heteroreceptors substantially reduces synaptic excitation of cholecystokinin-expressing interneurons in area CA1 of the rat hippocampus, in contrast to parvalbumin-expressing basket cells. The reduction is input specific, affecting only glutamatergic synaptic transmission originating from CA1 pyramidal cells. As a result, serotonin selectively decreases feedback inhibition via 5-HT(1B) receptor activation and subsequently increases the integration time window for spike generation in CA1 pyramidal cells. Our data imply an important role for serotonergic modulation of GABAergic action in subcortical control of hippocampal output.

AB - Midbrain raphe nuclei provide strong serotonergic projections to the hippocampus, in which serotonin (5-HT) exerts differential effects mediated by multiple 5-HT receptor subtypes. The functional relevance of this diversity of information processing is poorly understood. Here we show that serotonin via 5-HT(1B) heteroreceptors substantially reduces synaptic excitation of cholecystokinin-expressing interneurons in area CA1 of the rat hippocampus, in contrast to parvalbumin-expressing basket cells. The reduction is input specific, affecting only glutamatergic synaptic transmission originating from CA1 pyramidal cells. As a result, serotonin selectively decreases feedback inhibition via 5-HT(1B) receptor activation and subsequently increases the integration time window for spike generation in CA1 pyramidal cells. Our data imply an important role for serotonergic modulation of GABAergic action in subcortical control of hippocampal output.

KW - Animals

KW - Cholecystokinin

KW - Feedback, Physiological

KW - Female

KW - Glutamic Acid

KW - Hippocampus

KW - Immunohistochemistry

KW - Male

KW - Neural Inhibition

KW - Neural Pathways

KW - Neurons

KW - Patch-Clamp Techniques

KW - Raphe Nuclei

KW - Rats

KW - Rats, Wistar

KW - Serotonin

KW - Synaptic Transmission

KW - Journal Article

KW - Research Support, N.I.H., Extramural

KW - Research Support, Non-U.S. Gov't

U2 - 10.1523/JNEUROSCI.6382-10.2011

DO - 10.1523/JNEUROSCI.6382-10.2011

M3 - Article

C2 - 21653851

SN - 0270-6474

VL - 31

SP - 8464

EP - 8475

JO - Journal of Neuroscience

JF - Journal of Neuroscience

IS - 23

ER -

Cell-type-specific modulation of feedback inhibition by serotonin in the hippocampus

Abstract

Keywords / Materials (for Non-textual outputs)

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