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      Cell-Type-Specific Recruitment of Amygdala Interneurons to Hippocampal Theta Rhythm and Noxious Stimuli In Vivo

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          Summary

          Neuronal synchrony in the basolateral amygdala (BLA) is critical for emotional behavior. Coordinated theta-frequency oscillations between the BLA and the hippocampus and precisely timed integration of salient sensory stimuli in the BLA are involved in fear conditioning. We characterized GABAergic interneuron types of the BLA and determined their contribution to shaping these network activities. Using in vivo recordings in rats combined with the anatomical identification of neurons, we found that the firing of BLA interneurons associated with network activities was cell type specific. The firing of calbindin-positive interneurons targeting dendrites was precisely theta-modulated, but other cell types were heterogeneously modulated, including parvalbumin-positive basket cells. Salient sensory stimuli selectively triggered axo-axonic cells firing and inhibited firing of a disctinct projecting interneuron type. Thus, GABA is released onto BLA principal neurons in a time-, domain-, and sensory-specific manner. These specific synaptic actions likely cooperate to promote amygdalo-hippocampal synchrony involved in emotional memory formation.

          Highlights

          ► Comprehensive definition of interneuron types of the basolateral amygdala ► Identification of the target subcellular domains of each cell type ► GABAergic cell-type-specific coding of hippocampal theta rhythm and sensory stimuli ► Axo-axonic interneurons are excited by salient sensory stimuli

          Abstract

          Bienvenu et al. provide a comprehensive characterization and in vivo recordings of basolateral amygdala interneurons. Their findings suggest that GABA is released onto BLA principal neurons in a time-, subcellular domain-, and sensory-dependent manner.

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          Most cited references47

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          Neuronal synchrony: a versatile code for the definition of relations?

          W. Singer (1999)
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            Switching on and off fear by distinct neuronal circuits.

            Switching between exploratory and defensive behaviour is fundamental to survival of many animals, but how this transition is achieved by specific neuronal circuits is not known. Here, using the converse behavioural states of fear extinction and its context-dependent renewal as a model in mice, we show that bi-directional transitions between states of high and low fear are triggered by a rapid switch in the balance of activity between two distinct populations of basal amygdala neurons. These two populations are integrated into discrete neuronal circuits differentially connected with the hippocampus and the medial prefrontal cortex. Targeted and reversible neuronal inactivation of the basal amygdala prevents behavioural changes without affecting memory or expression of behaviour. Our findings indicate that switching between distinct behavioural states can be triggered by selective activation of specific neuronal circuits integrating sensory and contextual information. These observations provide a new framework for understanding context-dependent changes of fear behaviour.
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              Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition.

              The temporal resolution of neuronal integration depends on the time window within which excitatory inputs summate to reach the threshold for spike generation. Here, we show that in rat hippocampal pyramidal cells this window is very narrow (less than 2 milliseconds). This narrowness results from the short delay with which disynaptic feed-forward inhibition follows monosynaptic excitation. Simultaneous somatic and dendritic recordings indicate that feed-forward inhibition is much stronger in the soma than in the dendrites, resulting in a broader integration window in the latter compartment. Thus, the subcellular partitioning of feed-forward inhibition enforces precise coincidence detection in the soma, while allowing dendrites to sum incoming activity over broader time windows.
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                Author and article information

                Journal
                Neuron
                Neuron
                Neuron
                Cell Press
                0896-6273
                1097-4199
                21 June 2012
                21 June 2012
                : 74-20
                : 6
                : 1059-1074
                Affiliations
                [1 ]Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3TH, UK
                [2 ]Department of Pharmacology, Innsbruck Medical University, Peter Mayr Str. 1a, A-6020 Innsbruck, Austria
                Author notes
                []Corresponding author marco.capogna@ 123456pharm.ox.ac.uk
                [∗∗ ]Corresponding author thomas.bienvenu@ 123456inserm.fr
                [3]

                Present address: INSERM U862, Neurocentre Magendie, 146 rue Léo Saignat, 33077 Bordeaux, France

                Article
                NEURON11124
                10.1016/j.neuron.2012.04.022
                3391683
                22726836
                702b1385-45f7-45b5-b0ad-0686f056a8f6
                © 2012 ELL & Excerpta Medica.

                This document may be redistributed and reused, subject to certain conditions.

                History
                : 27 April 2012
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                Neurosciences
                Neurosciences

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