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      Pioneer glutamatergic cells develop into a morpho-functionally distinct population in the juvenile CA3 hippocampus

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          Abstract

          The developing CA3 hippocampus is comprised by highly connected hub neurons that are particularly effective in achieving network synchronization. Functional hub neurons were shown to be exclusively GABAergic, suggesting that the contribution of glutamatergic neurons to physiological synchronization processes at early postnatal stages is minimal. However, without fast GABAergic transmission, a different situation may prevail. In the adult CA3, blocking fast GABAergic transmission induces the generation of network bursts that can be triggered by the stimulation of single pyramidal neurons. Here we revisit the network function of CA3 glutamatergic neurons from a developmental viewpoint, without fast GABAergic transmission. We uncover a sub-population of early-generated glutamatergic neurons that impacts network dynamics when stimulated in the juvenile hippocampus. Additionally, this population displays characteristic morpho-physiological features in the juvenile and adult hippocampus. Therefore, the apparently homogeneous glutamatergic cell population likely displays a morpho-functional diversity rooted in temporal embryonic origins.

          Abstract

          The heterogeneity of cortical interneurons results from spatio-temporal differences in embryonic origin. Marissal et al. show that early-generated glutamatergic neurons display distinct morpho-functional features, suggesting that temporal factors are also important in determining glutamatergic function.

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          Most cited references39

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          Bursts as a unit of neural information: making unreliable synapses reliable.

          J E Lisman (1997)
          Several lines of evidence indicate that brief (< 25 ms) bursts of high-frequency firing have special importance in brain function. Recent work shows that many central synapses are surprisingly unreliable at signaling the arrival of single presynaptic action potentials to the postsynaptic neuron. However, bursts are reliably signaled because transmitter release is facilitated. Thus, these synapses can be viewed as filters that transmit bursts, but filter out single spikes. Bursts appear to have a special role in synaptic plasticity and information processing. In the hippocampus, a single burst can produce long-term synaptic modifications. In brain structures whose computational role is known, action potentials that arrive in bursts provide more-precise information than action potentials that arrive singly. These results, and the requirement for multiple inputs to fire a cell suggest that the best stimulus for exciting a cell (that is, a neural code) is coincident bursts.
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            Mechanisms of gamma oscillations in the hippocampus of the behaving rat.

            Gamma frequency oscillations (30-100 Hz) have been suggested to underlie various cognitive and motor functions. Here, we examine the generation of gamma oscillation currents in the hippocampus, using two-dimensional, 96-site silicon probes. Two gamma generators were identified, one in the dentate gyrus and another in the CA3-CA1 regions. The coupling strength between the two oscillators varied during both theta and nontheta states. Both pyramidal cells and interneurons were phase-locked to gamma waves. Anatomical connectivity, rather than physical distance, determined the coupling strength of the oscillating neurons. CA3 pyramidal neurons discharged CA3 and CA1 interneurons at latencies indicative of monosynaptic connections. Intrahippocampal gamma oscillation emerges in the CA3 recurrent system, which entrains the CA1 region via its interneurons.
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              The temporal and spatial origins of cortical interneurons predict their physiological subtype.

              Interneurons of the cerebral cortex represent a heterogeneous population of cells with important roles in network function. At present, little is known about how these neurons are specified in the developing telencephalon. To explore whether this diversity is established in the early progenitor populations, we conducted in utero fate-mapping of the mouse medial and caudal ganglionic eminences (MGE and CGE, respectively), from which most cortical interneurons arise. Mature interneuron subtypes were assessed by electrophysiological and immunological analysis, as well as by morphological reconstruction. At E13.5, the MGE gives rise to fast-spiking (FS) interneurons, whereas the CGE generates predominantly regular-spiking interneurons (RSNP). Later at E15.5, the CGE produces RSNP classes distinct from those generated from the E13.5 CGE. Thus, we provide evidence that the spatial and temporal origin of interneuron precursors in the developing telencephalic eminences predicts the intrinsic physiological properties of mature interneurons.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Pub. Group
                2041-1723
                27 December 2012
                : 3
                : 1316
                Affiliations
                [1 ]Inserm Unité 901 , Marseille 13009, France
                [2 ]Université de la Méditerranée, UMR S901 Aix-Marseille 2 , Marseille 13009, France
                [3 ]INMED , Marseille 13009, France
                [4 ]School of Physics and Astronomy, Tel Aviv University , Tel Aviv 69978, Israel
                [5 ]Departments of Physiology and Neuroscience, and Neural Science, and Langone Medical Center, New York University Neuroscience Institute , New York, New York 10016, USA
                [6 ]These authors contributed equally to this work
                Author notes
                Article
                ncomms2318
                10.1038/ncomms2318
                3535425
                23271650
                0db9d24f-baea-4148-9f67-ead298d4f665
                Copyright © 2012, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/

                History
                : 10 April 2012
                : 22 November 2012
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