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Hippocampal Theta Input to the Amygdala Shapes Feedforward Inhibition to Gate Heterosynaptic Plasticity

The dynamic interactions between hippocampus and amygdala are critical for emotional memory. Theta synchrony between these structures occurs during fear memory retrieval and may facilitate synaptic plasticity, but the cellular mechanisms are unknown. We report that interneurons of the mouse basal am... Full description

Journal Title: Neuron 2015, Vol.87 (6), p.1290-1303
Main Author: Bazelot, Michaël
Other Authors: Bocchio, Marco , Kasugai, Yu , Fischer, David , Dodson, Paul D , Ferraguti, Francesco , Capogna, Marco
Format: Electronic Article Electronic Article
Language: English
Subjects:
Quelle: Alma/SFX Local Collection
Publisher: United States: Elsevier Inc
ID: ISSN: 0896-6273
Link: https://www.ncbi.nlm.nih.gov/pubmed/26402610
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recordid: cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4590554
title: Hippocampal Theta Input to the Amygdala Shapes Feedforward Inhibition to Gate Heterosynaptic Plasticity
format: Article
creator:
  • Bazelot, Michaël
  • Bocchio, Marco
  • Kasugai, Yu
  • Fischer, David
  • Dodson, Paul D
  • Ferraguti, Francesco
  • Capogna, Marco
subjects:
  • Amygdala - physiology
  • Amygdala - ultrastructure
  • Animals
  • Article
  • Experiments
  • Hippocampus - physiology
  • Hippocampus - ultrastructure
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • nervous system
  • Neural Inhibition - physiology
  • Neuronal Plasticity - physiology
  • Neurons
  • Neuroscience(all)
  • Rodents
  • Synapses - physiology
  • Synapses - ultrastructure
  • Theta Rhythm - physiology
ispartof: Neuron, 2015, Vol.87 (6), p.1290-1303
description: The dynamic interactions between hippocampus and amygdala are critical for emotional memory. Theta synchrony between these structures occurs during fear memory retrieval and may facilitate synaptic plasticity, but the cellular mechanisms are unknown. We report that interneurons of the mouse basal amygdala are activated during theta network activity or optogenetic stimulation of ventral CA1 pyramidal cell axons, whereas principal neurons are inhibited. Interneurons provide feedforward inhibition that transiently hyperpolarizes principal neurons. However, synaptic inhibition attenuates during theta frequency stimulation of ventral CA1 fibers, and this broadens excitatory postsynaptic potentials. These effects are mediated by GABAB receptors and change in the Cl− driving force. Pairing theta frequency stimulation of ventral CA1 fibers with coincident stimuli of the lateral amygdala induces long-term potentiation of lateral-basal amygdala excitatory synapses. Hence, feedforward inhibition, known to enforce temporal fidelity of excitatory inputs, dominates hippocampus-amygdala interactions to gate heterosynaptic plasticity. [Display omitted] •Theta stimulation of CA1 ventral hippocampal fibers activates amygdala interneurons•Interneurons induce feedforward inhibition that hyperpolarizes principal neurons•Theta-evoked inhibition attenuates to broaden excitation on principal neurons•Feedforward inhibition gates heterosynaptic plasticity via GABAB receptors Hippocampal-amygdala interactions are critical for emotional memory, but the cellular mechanisms are unknown. In this paper, Bazelot, Bocchio et al. functionally demonstrate that GABAergic neurons of the basal amygdala gate principal neuron firing and heterosynaptic plasticity in the mouse amygdala.
language: eng
source: Alma/SFX Local Collection
identifier: ISSN: 0896-6273
fulltext: fulltext
issn:
  • 0896-6273
  • 1097-4199
url: Link


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descriptionThe dynamic interactions between hippocampus and amygdala are critical for emotional memory. Theta synchrony between these structures occurs during fear memory retrieval and may facilitate synaptic plasticity, but the cellular mechanisms are unknown. We report that interneurons of the mouse basal amygdala are activated during theta network activity or optogenetic stimulation of ventral CA1 pyramidal cell axons, whereas principal neurons are inhibited. Interneurons provide feedforward inhibition that transiently hyperpolarizes principal neurons. However, synaptic inhibition attenuates during theta frequency stimulation of ventral CA1 fibers, and this broadens excitatory postsynaptic potentials. These effects are mediated by GABAB receptors and change in the Cl− driving force. Pairing theta frequency stimulation of ventral CA1 fibers with coincident stimuli of the lateral amygdala induces long-term potentiation of lateral-basal amygdala excitatory synapses. Hence, feedforward inhibition, known to enforce temporal fidelity of excitatory inputs, dominates hippocampus-amygdala interactions to gate heterosynaptic plasticity. [Display omitted] •Theta stimulation of CA1 ventral hippocampal fibers activates amygdala interneurons•Interneurons induce feedforward inhibition that hyperpolarizes principal neurons•Theta-evoked inhibition attenuates to broaden excitation on principal neurons•Feedforward inhibition gates heterosynaptic plasticity via GABAB receptors Hippocampal-amygdala interactions are critical for emotional memory, but the cellular mechanisms are unknown. In this paper, Bazelot, Bocchio et al. functionally demonstrate that GABAergic neurons of the basal amygdala gate principal neuron firing and heterosynaptic plasticity in the mouse amygdala.
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subjectAmygdala - physiology ; Amygdala - ultrastructure ; Animals ; Article ; Experiments ; Hippocampus - physiology ; Hippocampus - ultrastructure ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; nervous system ; Neural Inhibition - physiology ; Neuronal Plasticity - physiology ; Neurons ; Neuroscience(all) ; Rodents ; Synapses - physiology ; Synapses - ultrastructure ; Theta Rhythm - physiology
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descriptionThe dynamic interactions between hippocampus and amygdala are critical for emotional memory. Theta synchrony between these structures occurs during fear memory retrieval and may facilitate synaptic plasticity, but the cellular mechanisms are unknown. We report that interneurons of the mouse basal amygdala are activated during theta network activity or optogenetic stimulation of ventral CA1 pyramidal cell axons, whereas principal neurons are inhibited. Interneurons provide feedforward inhibition that transiently hyperpolarizes principal neurons. However, synaptic inhibition attenuates during theta frequency stimulation of ventral CA1 fibers, and this broadens excitatory postsynaptic potentials. These effects are mediated by GABAB receptors and change in the Cl− driving force. Pairing theta frequency stimulation of ventral CA1 fibers with coincident stimuli of the lateral amygdala induces long-term potentiation of lateral-basal amygdala excitatory synapses. Hence, feedforward inhibition, known to enforce temporal fidelity of excitatory inputs, dominates hippocampus-amygdala interactions to gate heterosynaptic plasticity. [Display omitted] •Theta stimulation of CA1 ventral hippocampal fibers activates amygdala interneurons•Interneurons induce feedforward inhibition that hyperpolarizes principal neurons•Theta-evoked inhibition attenuates to broaden excitation on principal neurons•Feedforward inhibition gates heterosynaptic plasticity via GABAB receptors Hippocampal-amygdala interactions are critical for emotional memory, but the cellular mechanisms are unknown. In this paper, Bazelot, Bocchio et al. functionally demonstrate that GABAergic neurons of the basal amygdala gate principal neuron firing and heterosynaptic plasticity in the mouse amygdala.
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titleHippocampal Theta Input to the Amygdala Shapes Feedforward Inhibition to Gate Heterosynaptic Plasticity
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abstractThe dynamic interactions between hippocampus and amygdala are critical for emotional memory. Theta synchrony between these structures occurs during fear memory retrieval and may facilitate synaptic plasticity, but the cellular mechanisms are unknown. We report that interneurons of the mouse basal amygdala are activated during theta network activity or optogenetic stimulation of ventral CA1 pyramidal cell axons, whereas principal neurons are inhibited. Interneurons provide feedforward inhibition that transiently hyperpolarizes principal neurons. However, synaptic inhibition attenuates during theta frequency stimulation of ventral CA1 fibers, and this broadens excitatory postsynaptic potentials. These effects are mediated by GABAB receptors and change in the Cl− driving force. Pairing theta frequency stimulation of ventral CA1 fibers with coincident stimuli of the lateral amygdala induces long-term potentiation of lateral-basal amygdala excitatory synapses. Hence, feedforward inhibition, known to enforce temporal fidelity of excitatory inputs, dominates hippocampus-amygdala interactions to gate heterosynaptic plasticity. [Display omitted] •Theta stimulation of CA1 ventral hippocampal fibers activates amygdala interneurons•Interneurons induce feedforward inhibition that hyperpolarizes principal neurons•Theta-evoked inhibition attenuates to broaden excitation on principal neurons•Feedforward inhibition gates heterosynaptic plasticity via GABAB receptors Hippocampal-amygdala interactions are critical for emotional memory, but the cellular mechanisms are unknown. In this paper, Bazelot, Bocchio et al. functionally demonstrate that GABAergic neurons of the basal amygdala gate principal neuron firing and heterosynaptic plasticity in the mouse amygdala.
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