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      Subplate Cells: Amplifiers of Neuronal Activity in the Developing Cerebral Cortex

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          Abstract

          Due to their unique structural and functional properties, subplate cells are ideally suited to function as important amplifying units within the developing neocortical circuit. Subplate neurons have extensive dendritic and axonal ramifications and relatively mature functional properties, i.e. their action potential firing can exceed frequencies of 40 Hz. At earliest stages of corticogenesis subplate cells receive functional synaptic inputs from the thalamus and from other cortical and non-cortical sources. Glutamatergic and depolarizing GABAergic inputs arise from cortical neurons and neuromodulatory inputs arise from the basal forebrain and other sources. Activation of postsynaptic metabotropic receptors, i.e. muscarinic receptors, elicits in subplate neurons oscillatory burst discharges which are transmitted via electrical and chemical synapses to neighbouring subplate cells and to immature neurons in the cortical plate. The tonic non-synaptic release of GABA from GABAergic subplate cells facilitates the generation of burst discharges. These cellular bursts are amplified by prominent gap junction coupling in the subplate and cortical plate, thereby eliciting 10–20 Hz oscillations in a local columnar network. Thus, we propose that neuronal networks are organized at earliest stages in a gap junction coupled columnar syncytium. We postulate that the subplate does not only serve as a transient relay station for afferent inputs, but rather as an active element amplifying the afferent and intracortical activity.

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          GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations.

          Developing networks follow common rules to shift from silent cells to coactive networks that operate via thousands of synapses. This review deals with some of these rules and in particular those concerning the crucial role of the neurotransmitter gamma-aminobuytric acid (GABA), which operates primarily via chloride-permeable GABA(A) receptor channels. In all developing animal species and brain structures investigated, neurons have a higher intracellular chloride concentration at an early stage leading to an efflux of chloride and excitatory actions of GABA in immature neurons. This triggers sodium spikes, activates voltage-gated calcium channels, and acts in synergy with NMDA channels by removing the voltage-dependent magnesium block. GABA signaling is also established before glutamatergic transmission, suggesting that GABA is the principal excitatory transmitter during early development. In fact, even before synapse formation, GABA signaling can modulate the cell cycle and migration. The consequence of these rules is that developing networks generate primitive patterns of network activity, notably the giant depolarizing potentials (GDPs), largely through the excitatory actions of GABA and its synergistic interactions with glutamate signaling. These early types of network activity are likely required for neurons to fire together and thus to "wire together" so that functional units within cortical networks are formed. In addition, depolarizing GABA has a strong impact on synaptic plasticity and pathological insults, notably seizures of the immature brain. In conclusion, it is suggested that an evolutionary preserved role for excitatory GABA in immature cells provides an important mechanism in the formation of synapses and activity in neuronal networks.
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            A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution.

            The more than 1000-fold increase in the cortical surface without a comparable increase in its thickness during mammalian evolution is explained in the context of the radial-unit hypothesis of cortical development. According to the proposed model, cortical expansion is the result of changes in proliferation kinetics that increase the number of radial columnar units without changing the number of neurons within each unit significantly. Thus, mutation of a regulatory gene(s) that controls the timing and ratio of symmetric and asymmetric modes of cell divisions in the proliferative zone, coupled with radial constraints in the distribution of migrating neurons, could create an expanded cortical plate with enhanced capacity for establishing new patterns of connectivity that are validated through natural selection.
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              Development of the human cerebral cortex: Boulder Committee revisited.

              In 1970 the Boulder Committee described the basic principles of the development of the CNS, derived from observations on the human embryonic cerebrum. Since then, numerous studies have significantly advanced our knowledge of the timing, sequence and complexity of developmental events, and revealed important inter-species differences. We review current data on the development of the human cerebral cortex and update the classical model of how the structure that makes us human is formed.
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                Author and article information

                Journal
                Front Neuroanat
                Front. Neuroanat.
                Frontiers in Neuroanatomy
                Frontiers Research Foundation
                1662-5129
                25 July 2009
                07 October 2009
                2009
                : 3
                : 19
                Affiliations
                [1] 1simpleInstitute of Physiology and Pathophysiology, University Medical Center, Johannes Gutenberg University Mainz Mainz, Germany
                Author notes

                Edited by: Kathleen S. Rockland, RIKEN Brain Science Institute, Japan

                Reviewed by: Patrick Kanold, University of Maryland, USA; Ivica Kostovic, University of Zagreb, Croatia

                *Correspondence: Heiko J. Luhmann, Institute of Physiology and Pathophysiology, University of Mainz, Duesbergweg 6, D-55128 Mainz, Germany. e-mail: luhmann@ 123456uni-mainz.de

                Present address: Ileana L. Hanganu-Opatz, Center for Molecular Neurobiology, University Medical Center Hamburg-Eppendorf, Martinistr. 85, 20251 Hamburg, Germany.

                Article
                10.3389/neuro.05.019.2009
                2766272
                19862346
                ed5e6767-ae2d-425c-9476-a7d0179130bf
                Copyright © 2009 Luhmann, Kilb and Hanganu-Opatz.

                This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

                History
                : 07 July 2009
                : 04 September 2009
                Page count
                Figures: 8, Tables: 0, Equations: 0, References: 96, Pages: 11, Words: 8016
                Categories
                Neuroscience
                Review Article

                Neurosciences
                nmda,microciruitry,glutamate,gaba,electrophysiology,neocortex,subplate,development
                Neurosciences
                nmda, microciruitry, glutamate, gaba, electrophysiology, neocortex, subplate, development

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