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Controlling synchronization of gamma oscillations by astrocytic modulation in a model hippocampal neural network.

ABSTRACT: Recent in vitro and in vivo experiments demonstrate that astrocytes participate in the maintenance of cortical gamma oscillations and recognition memory. However, the mathematical understanding of the underlying dynamical mechanisms remains largely incomplete. Here we investigate how the interplay of slow modulatory astrocytic signaling with fast synaptic transmission controls coherent oscillations in the network of hippocampal interneurons that receive inputs from pyramidal cells. We show that the astrocytic regulation of signal transmission between neurons improves the firing synchrony and extends the region of coherent oscillations in the biologically relevant values of synaptic conductance. Astrocyte-mediated potentiation of inhibitory synaptic transmission markedly enhances the coherence of network oscillations over a broad range of model parameters. Astrocytic regulation of excitatory synaptic input improves the robustness of interneuron network gamma oscillations induced by physiologically relevant excitatory model drive. These findings suggest a mechanism, by which the astrocytes become involved in cognitive function and information processing through modulating fast neural network dynamics.

SUBMITTER: Makovkin S

PROVIDER: S-EPMC9050920 | biostudies-literature | 2022 Apr

REPOSITORIES: biostudies-literature

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Controlling synchronization of gamma oscillations by astrocytic modulation in a model hippocampal neural network.

Makovkin Sergey S Kozinov Evgeny E Ivanchenko Mikhail M Gordleeva Susanna S

Scientific reports 20220428 1

Recent in vitro and in vivo experiments demonstrate that astrocytes participate in the maintenance of cortical gamma oscillations and recognition memory. However, the mathematical understanding of the underlying dynamical mechanisms remains largely incomplete. Here we investigate how the interplay of slow modulatory astrocytic signaling with fast synaptic transmission controls coherent oscillations in the network of hippocampal interneurons that receive inputs from pyramidal cells. We show that ...[more]

PMID: 35484169

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Project description:BackgroundGamma oscillations are electric activity patterns of the mammalian brain hypothesized to serve attention, sensory perception, working memory and memory encoding. They are disrupted or altered in schizophrenic patients with associated cognitive deficits, which persist in spite of treatment with antipsychotics. Because cognitive symptoms are a core feature of schizophrenia it is relevant to explore signaling pathways that potentially regulate gamma oscillations. Dopamine has been reported to decrease gamma oscillation power via D1-like receptors. Based on the expression pattern of D4 receptors (D4R) in hippocampus, and pharmacological effects of D4R ligands in animals, we hypothesize that they are in a position to regulate gamma oscillations as well.Methodology/principal findingsTo address this hypothesis we use rat hippocampal slices and kainate-induced gamma oscillations. Local field potential recordings as well as intracellular recordings of pyramidal cells, fast-spiking and non-fast-spiking interneurons were carried out. We show that D4R activation with the selective ligand PD168077 increases gamma oscillation power, which can be blocked by the D4R-specific antagonist L745,870 as well as by the antipsychotic drug Clozapine. Pyramidal cells did not exhibit changes in excitatory or inhibitory synaptic current amplitudes, but inhibitory currents became more coherent with the oscillations after application of PD168077. Fast-spiking, but not non-fast spiking, interneurons, increase their action potential phase-coupling and coherence with regard to ongoing gamma oscillations in response to D4R activation. Among several possible mechanisms we found that the NMDA receptor antagonist AP5 also blocks the D4R mediated increase in gamma oscillation power.Conclusions/significanceWe conclude that D4R activation affects fast-spiking interneuron synchronization and thereby increases gamma power by an NMDA receptor-dependent mechanism. This suggests that converging deficits on fast-spiking interneurons may lead to decreased network function and thus aberrant gamma oscillations and cognitive decline in schizophrenia.

Project description:Fine-scale temporal organization of cortical activity in the gamma range (∼25-80Hz) may play a significant role in information processing, for example by neural grouping ('binding') and phase coding. Recent experimental studies have shown that the precise frequency of gamma oscillations varies with input drive (e.g. visual contrast) and that it can differ among nearby cortical locations. This has challenged theories assuming widespread gamma synchronization at a fixed common frequency. In the present study, we investigated which principles govern gamma synchronization in the presence of input-dependent frequency modulations and whether they are detrimental for meaningful input-dependent gamma-mediated temporal organization. To this aim, we constructed a biophysically realistic excitatory-inhibitory network able to express different oscillation frequencies at nearby spatial locations. Similarly to cortical networks, the model was topographically organized with spatially local connectivity and spatially-varying input drive. We analyzed gamma synchronization with respect to phase-locking, phase-relations and frequency differences, and quantified the stimulus-related information represented by gamma phase and frequency. By stepwise simplification of our models, we found that the gamma-mediated temporal organization could be reduced to basic synchronization principles of weakly coupled oscillators, where input drive determines the intrinsic (natural) frequency of oscillators. The gamma phase-locking, the precise phase relation and the emergent (measurable) frequencies were determined by two principal factors: the detuning (intrinsic frequency difference, i.e. local input difference) and the coupling strength. In addition to frequency coding, gamma phase contained complementary stimulus information. Crucially, the phase code reflected input differences, but not the absolute input level. This property of relative input-to-phase conversion, contrasting with latency codes or slower oscillation phase codes, may resolve conflicting experimental observations on gamma phase coding. Our modeling results offer clear testable experimental predictions. We conclude that input-dependency of gamma frequencies could be essential rather than detrimental for meaningful gamma-mediated temporal organization of cortical activity.

Dataset Information

Controlling synchronization of gamma oscillations by astrocytic modulation in a model hippocampal neural network.

Publications

Controlling synchronization of gamma oscillations by astrocytic modulation in a model hippocampal neural network.

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