Physiological effects of sustained blockade of excitatory synaptic transmission on spontaneously active developing neuronal networks—an inquiry into the reciprocal linkage between intrinsic biorhythms and neuroplasticity in early ontogeny

Corner, M.A.; Pelt, Jaap van; Wolters, P.S.; Baker, Robert E.; Nuytinck, R.H

doi:10.1016/s0149-7634(01)00062-8

Cited by 124 publications

(180 citation statements)

References 770 publications

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“…Using recordings from single networks over the course of 6 weeks, the present study extends these observations and demonstrates that neuronal avalanches are a robust form of neuronal synchronization that occurs throughout postnatal development. Large changes in activity levels have been reported previously for organotypic slice cultures during postnatal maturation (Maeda, Robinson et al, 1995;Kamioka, Maeda et al, 1996;Corner, van Pelt et al, 2002;Johnson and Buonomano, 2007) and are also found in our study. Importantly, we show that despite these changes in activity levels, the organization of synchronization in the form of neuronal avalanches remains constant for many weeks even in single cultures.…”

Section: The Organization Of Spontaneous Synchronized Activity In Orgsupporting

confidence: 91%

“…The typical neuronal activity in this in vitro system has been characterized by brief periods of activity separated by many seconds of quiescence and has been given various labels that highlight different aspects such as the abrupt and brief nature of activity periods ('bursts' or 'Spikes'), their non-oscillatory recurrence ('irregular'), their overlap in time at different cortical sites ('synchronous'), or their propagation, i.e. successive initiation at different sites ('waves') (Crain, 1966;Calvet, 1974;Dichter, 1978;Plenz and Aertsen, 1996a;Plenz and Aertsen, 1996b;Gorba, Klostermann et al, 1999;Klostermann and Wahle, 1999;Corner, van Pelt et al, 2002;Eytan and Marom, 2006). Using extracellular local field potentials (LFP), which are particularly well suited to study network states as they correlate with synchronized activity of local neuronal populations in vivo (Arieli, 1992;Lampl, Reichova et al, 1999), we demonstrated recently that the spontaneous LFPs in isolated cortical networks are ordered such that the probability P of a spatiotemporal LFP cluster of size s follows a power law…”

Section: Introductionmentioning

confidence: 99%

“…These cultures transition through different activity levels during postnatal maturation (Maeda, Robinson et al, 1995;Kamioka, Maeda et al, 1996;Corner, van Pelt et al, 2002;Johnson and Buonomano, 2007) and are well suited to identify a common network state that encompasses the variable features of the overall activity. We show that a power law with an exponent of α = −1.5, i.e.…”

Section: Introductionmentioning

confidence: 99%

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Homeostasis of neuronal avalanches during postnatal cortex development in vitro

Stewart

Plenz

2008

Journal of Neuroscience Methods

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Cortical networks in vivo and in vitro are spontaneously active in the absence of inputs, generating highly variable bursts of neuronal activity separated by up to seconds of quiescence. Previous measurements in adult rat cortex revealed an intriguing underlying organization of these dynamics, termed neuronal avalanches, which is indicative of a critical network state. Here we demonstrate that neuronal avalanches persist throughout development in cortical slice cultures from newborn rats. More specifically, we find that in spite of large variations of average rate in activity, spontaneous bursts occur with power-law distributed sizes (exponent -1.5) and a critical branching parameter close to 1. Our findings suggest that cortical networks homeostatically regulate a critical state during postnatal maturation.

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Section: The Organization Of Spontaneous Synchronized Activity In Orgsupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Homeostasis of neuronal avalanches during postnatal cortex development in vitro

Stewart

Plenz

2008

Journal of Neuroscience Methods

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“…Multi-electrode arrays (MEAs) have also been extensively used to probe cultured neural networks (Corner et al, 2002;Pasquale et al, 2008;Wagenaar et al, 2005), namely to characterize the bursting activity in developing cultured neural networks and control activity in these networks by stimulating at different electrode sites (Madhavan et al, 2006;Massobrio et al, 2007;Wagenaar et al, 2005). However, the extracellular stimulation from the array suffers from poor spatial localization (Heuschkel et al, 2002) and stimulation artifacts (Wagenaar and Potter, 2004).…”

Section: Discussionmentioning

confidence: 99%

Laser-evoked synaptic transmission in cultured hippocampal neurons expressing channelrhodopsin-2 delivered by adeno-associated virus

Wang¹,

Hasan²,

Seung³

2009

Journal of Neuroscience Methods

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We present a method for studying synaptic transmission in mass cultures of dissociated hippocampal neurons based on patch clamp recording combined with laser stimulation of neurons expressing Channelrhodopsin-2 (ChR2). Our goal was to use the high spatial resolution of laser illumination to come as close as possible to the ideal of identifying monosynaptically coupled pairs of neurons, which is conventionally done using microisland rather than mass cultures. Using recombinant adenoassociated virus (rAAV) to deliver the ChR2 gene, we focused on the time period between 14 and 20 days in vitro, during which expression levels are high, and spontaneous bursting activity has not yet started. Stimulation by wide-field illumination is sufficient to make the majority of ChR2-expressing neurons spike. Stimulation with a laser spot at least 10 μm in diameter also produces action potentials, but in a reduced fraction of neurons. We studied synaptic transmission by voltageclamping a neuron with low expression of ChR2 and scanning a 40 μm laser spot at surrounding locations. Responses were observed to stimulation at a subset of locations in the culture, indicating spatial localization of stimulation. Pharmacological means were used to identify responses that were synaptic. Many responses were of smaller amplitude than those typically found in microisland cultures. We were unable to find an entirely reliable criterion for distinguishing between monosynaptic and polysynaptic responses. However, we propose that postsynaptic currents with Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. HHMI Author ManuscriptHHMI Author Manuscript HHMI Author Manuscript small amplitudes, simple shapes, and latencies not much greater than 8 msec are reasonable candidates for monosynaptic interactions.

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“…We report here that this homeostatic return of spontaneous, now kainate receptor driven, firing is accompanied by a reciprocal down-regulation of the blocked AMPA and NMDA receptors, such that the developing cortical network is protected from becoming hyperactive when these synaptic inputs again become able to transmit normally.Intrinsically generated bioelectric currents, periodically triggering polyneuronal bursts and isolated spikes, is a well-nigh universal feature of neural networks, especially during early ontogeny [1]. Spontaneous burst activity (SBA) is characteristically organized as nested clusters of action potentials on increasingly higher order time-scales, which show a strong capacity for reacting homeostatically to experimental interference [2].…”

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confidence: 99%

Reciprocal homeostatic reactions to chronic excitatory synaptic receptor inactivation in developing cerebral cortex networks

Corner¹

2007

Nature Precedings

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Chronic blockade of excitatory glutamatergic synaptic receptors in co-cultured organotypic rodent neocortex explants leads to a compensatory up-regulation of otherwise inactive input channels so as to maintain almost normal levels of ongoing bursts of action potentials. We report here that this homeostatic return of spontaneous, now kainate receptor driven, firing is accompanied by a reciprocal down-regulation of the blocked AMPA and NMDA receptors, such that the developing cortical network is protected from becoming hyperactive when these synaptic inputs again become able to transmit normally.Intrinsically generated bioelectric currents, periodically triggering polyneuronal bursts and isolated spikes, is a well-nigh universal feature of neural networks, especially during early ontogeny [1]. Spontaneous burst activity (SBA) is characteristically organized as nested clusters of action potentials on increasingly higher order time-scales, which show a strong capacity for reacting homeostatically to experimental interference [2]. Thus, NMDA receptor blockade in developing organotypic rodent visual cortex cultures begins within hours to be compensated for by steadily rising firing rates, which regain stable control levels within 24h [1,2]. Although action potential discharges are then purely AMPA receptor driven, 2-weekold chronically treated cultures show no augmentation of spontaneous activity, and continue to burst normally, upon release of their NMDA receptors from the pharmacological blockade.Combined blockade of NMDA and AMPA receptors eliminates SBA throughout the treatment period in isolated cortex cultures [1] but fails to do so in co-cultured explants which have been enabled to cross-innervate one another [3]. In such preparations, kainate receptormediated SBA takes over for the blocked excitatory receptors [2], as could be shown by acute application of the highly selective kainate blocker LY382284 (courtesy of Eli Lilly & Co). Spontaneous firing levels and burst intensities failed to be fully restored, however, primarily owing to a dearth of exceptionally active explants in the experimental group (see table 1: 'growth medium'). When such cultures were subsequently assayed in control medium the treated explants became more active (table 1) but, here too, did not exceed the values recorded in the control group. Although spontaneous bursts tended to be somewhat longer than normal, they were correspondingly less frequent and intense [4]. Three-week-old cultures gave comparable results, on the whole, but were much more individually variable.One might have expected that even if, by virtue of the homeostatic restoration of SBA, blocked glutamate receptors had been prevented from becoming sensitized (and inhibitory interneurons from declining in number and/or efficacy) during the treatment period, they still ought to have contributed to intensified spontaneous firing when acting in synergy with the up-regulated kainate receptors. Their failure to do so suggests that, in accordance with a 'Hebbian' weakening of ina...

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Physiological effects of sustained blockade of excitatory synaptic transmission on spontaneously active developing neuronal networks—an inquiry into the reciprocal linkage between intrinsic biorhythms and neuroplasticity in early ontogeny

Cited by 124 publications

References 770 publications

Homeostasis of neuronal avalanches during postnatal cortex development in vitro

Homeostasis of neuronal avalanches during postnatal cortex development in vitro

Laser-evoked synaptic transmission in cultured hippocampal neurons expressing channelrhodopsin-2 delivered by adeno-associated virus

Reciprocal homeostatic reactions to chronic excitatory synaptic receptor inactivation in developing cerebral cortex networks

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