A Homeostatic Model of Neuronal Firing Governed by Feedback Signals from the Extracellular Matrix

Kazantsev, Victor B.; Gordleeva, Susanna; Stasenko, Sergey V.; Dityatev, Alexander

doi:10.1371/journal.pone.0041646

Cited by 33 publications

(36 citation statements)

References 25 publications

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“…For intrinsic learning it has often been assumed that it may implement purely homeostatic adaptation [26,27,28,29,30], but see also [31]. Experimental results are often inconsistent [32,33,34,4,35,36,37,38].…”

Section: Introductionmentioning

confidence: 99%

Logarithmic distributions prove that intrinsic learning is Hebbian

Scheler¹

2017

F1000Res

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In this paper, we document lognormal distributions for spike rates, synaptic weights and intrinsic excitability (gain) for neurons in various brain areas, such as auditory or visual cortex, hippocampus, cerebellum, striatum, midbrain nuclei. We find a remarkable consistency of heavy-tailed, specifically lognormal, distributions for rates, weights and gains in all brain areas. The difference between strongly recurrent and feed-forward connectivity (cortex vs. striatum and cerebellum), neurotransmitter (GABA (striatum) or glutamate (cortex)) or the level of activation (low in cortex, high in Purkinje cells and midbrain nuclei) turns out to be irrelevant for this feature. Logarithmic scale distribution of weights and gains appears as a functional property that is present everywhere. Secondly, we created a generic neural model to show that Hebbian learning will create and maintain lognormal distributions. We could prove with the model that not only weights, but also intrinsic gains, need to have strong Hebbian learning in order to produce and maintain the experimentally attested distributions. This settles a long-standing question about the type of plasticity exhibited by intrinsic excitability.

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Section: Introductionmentioning

confidence: 99%

Logarithmic distributions prove that intrinsic learning is Hebbian

Scheler¹

2017

F1000Res

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“…Furthermore, the injection of Hyase before contextual fear conditioning impairs the formation/retention of fear memories. A mathematical modeling study highlighted that the ECM may function as a memory substrate by showing that remodeling of ECM may lead to a bistability in which two different stable levels of average firing rates can coexist in a spiking network (Kazantsev et al, 2012). The multiple roles played by the ECM in healthy brain neuroplasticity suggest that it could be an important factor for pathogenic plasticity associated with epileptogenesis (Dityatev, 2010), which results in the transformation of normal neuronal network activity into spontaneous recurrent epileptiform discharges (seizures; Robert et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

Seizure-like activity in hyaluronidase-treated dissociated hippocampal cultures

Vedunova¹,

Сахарнова²,

Митрошина³

et al. 2013

Front. Cell. Neurosci.

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The extracellular matrix (ECM) plays an important role in use-dependent synaptic plasticity. Hyaluronic acid (HA) is the backbone of the neural ECM, which has been shown to modulate α-amino-3-hydroxyl-5-methyl-4-isoxazolepropionate (AMPA) receptor mobility, paired-pulse depression, L-type voltage-dependent Ca2+ channel (L-VDCC) activity, long-term potentiation and contextual fear conditioning. To investigate the role of HA in the development of spontaneous neuronal network activity, we used microelectrode array recording and Ca2+ imaging in hippocampal cultures enzymatically treated with hyaluronidase. Our findings revealed an appearance of epileptiform activity 9 days after hyaluronidase treatment. The treatment transformed the normal network firing bursts and Ca2+ oscillations into long-lasting “superbursts” and “superoscillations” with durations of 11–100 s. The changes in Ca2+ transients in hyaluronidase-treated neurons were more prominent then in astrocytes and preceded changes in electrical activity. The Ca2+ superoscillations could be suppressed by applying the L-VDCC blocker diltiazem, whereas the neuronal firing superbursts could be additionally suppressed by 6-cyano-7-nitroquinoxaline-2,3-dione as an antagonist of AMPA/kainate receptors. These results suggest that changes in the expression of HA can be epileptogenic and that hyaluronidase treatment in vitro provides a robust model for the dissection of the underlying mechanisms.

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“…In fact, compartmentalization of this feedback component outside of the cell may be an advantage for networkwide regulation or prevention of interference in other intracellular pathways. CSPGs and associated ECM molecules are candidates for this kind of long-term homeostatic regulation, as shown in recent theoretical work (Kazantsev et al 2012).…”

mentioning

confidence: 84%

Degradation of extracellular chondroitin sulfate delays recovery of network activity after perturbation

Hudson

Gollnick

Gourdine

et al. 2015

Journal of Neurophysiology

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Hudson AE, Gollnick C, Gourdine JP, Prinz AA. Degradation of extracellular chondroitin sulfate delays recovery of network activity after perturbation. J Neurophysiol 114: 1346 -1352, 2015. First published June 24, 2015 doi:10.1152/jn.00455.2015.-Chondroitin sulfate proteoglycans (CSPGs) are widely studied in vertebrate systems and are known to play a key role in development, plasticity, and regulation of cortical circuitry. The mechanistic details of this role are still elusive, but increasingly central to the investigation is the homeostatic balance between network excitation and inhibition. Studying a simpler neuronal circuit may prove advantageous for discovering the mechanistic details of the cellular effects of CSPGs. In this study we used a well-established model of homeostatic change after injury in the crab Cancer borealis to show first evidence that CSPGs are necessary for network activity homeostasis. We degraded CSPGs in the pyloric circuit of the stomatogastric ganglion with the enzyme chondroitinase ABC (chABC) and found that removal of CSPGs does not influence the ongoing rhythm of the pyloric circuit but does limit its capacity for recovery after a networkwide perturbation. Without CSPGs, the postperturbation rhythm is slower than in controls and rhythm recovery is delayed. In addition to providing a new model system for the study of CSPGs, this study suggests a wider role for CSPGs, and perhaps the extracellular matrix in general, beyond simply plastic reorganization (as observed in mammals) and into a foundational regulatory role of neural circuitry.

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A Homeostatic Model of Neuronal Firing Governed by Feedback Signals from the Extracellular Matrix

Cited by 33 publications

References 25 publications

Logarithmic distributions prove that intrinsic learning is Hebbian

Logarithmic distributions prove that intrinsic learning is Hebbian

Seizure-like activity in hyaluronidase-treated dissociated hippocampal cultures

Degradation of extracellular chondroitin sulfate delays recovery of network activity after perturbation

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