Role of GABAergic inhibition in hippocampal network oscillations

Mann, Edward O.; Paulsen, Ole

doi:10.1016/j.tins.2007.05.003

Cited by 350 publications

(309 citation statements)

References 69 publications

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“…Several findings support the view that these cortical activities reflect the synchronization of inhibitory GABAergic networks (see Traub et al, 1999;Whittington and Traub, 2003;Mann and Paulsen, 2007), with or without the contribution of excitatory glutamatergic networks (Bartos et al, 2007). For instance, gamma activities induced by the cholinergic agonist carbachol are abolished or greatly diminished by GABA A receptor (Fig.…”

Section: Role Of Gaba a Receptors In Neuronal Network Oscillationssupporting

confidence: 64%

GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity

Avoli¹,

Curtis²

2011

Progress in Neurobiology

224

253

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GABA is the main inhibitory neurotransmitter in the adult forebrain, where it activates ionotropic type A and metabotropic type B receptors. Early studies have shown that GABA A receptormediated inhibition controls neuronal excitability and thus the occurrence of seizures. However, more complex, and at times unexpected, mechanisms of GABAergic signaling have been identified during epileptiform discharges over the last few years. Here, we will review experimental data that point at the paradoxical role played by GABA A receptor-mediated mechanisms in synchronizing neuronal networks, and in particular those of limbic structures such as the hippocampus, the entorhinal and perirhinal cortices, or the amygdala. After having summarized the fundamental characteristics of GABA A receptor-mediated mechanisms, we will analyze their role in the generation of network oscillations and their contribution to epileptiform synchronization. Whether and how GABA A receptors influence the interaction between limbic networks leading to ictogenesis will be also reviewed. Finally, we will consider the role of altered inhibition in the human epileptic brain along with the ability of GABA A receptor-mediated conductances to generate synchronous depolarizing events that may lead to ictogenesis in human epileptic disorders as well.

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Section: Role Of Gaba a Receptors In Neuronal Network Oscillationssupporting

confidence: 64%

GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity

Avoli¹,

Curtis²

2011

Progress in Neurobiology

224

253

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“…Recent evidence suggests that autaptic synapses from PV-staining interneurons regulates the spike timing of both the interneurons themselves and the pyramidal cells they synapse with (Bacci and Huguenard, 2006). Indeed, GABA A -receptor mediated hyperpolarization is known to phase-reset principal neuron oscillations, which would have the precise effect of increasing phase-locking to stimuli (e.g., see Mann and Paulsen, 2007).…”

Section: Discussionmentioning

confidence: 99%

Cortical source estimates of gamma band amplitude and phase are different in schizophrenia

et al. 2008

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Reductions in gamma band phase synchrony and evoked power have been reported in schizophrenic subjects in response to auditory stimuli. These results have been observed in the EEG at one or two electrode sites. We wished to extend these results using magnetic field data to estimate the responses at the neural generators themselves in each hemisphere. Whole head magnetoencephalographic (MEG) recordings were used to estimate the phase and amplitude behavior of sources in primary auditory cortex in both hemispheres of schizophrenic and comparison subjects. Both ipsi-and contralateral cases were evaluated using a driving (40 Hz modulated 1 kHz carrier) and a non-driving (1 kHz tone) stimulus. We used source space projection (SSP) to collapse the magnetic field data into estimates of the time course of source strengths in individual trials. Complex wavelet based timefrequency decomposition was used to compute inter-trial phase locking factor (PLF), and mean evoked and induced amplitude for each cortical generator. Schizophrenic subjects showed reduced SSP PLF and evoked source strength for contra-lateral generators responding to the driving stimulus in both hemispheres. For the pure tone stimulus, only the left hemisphere PLF's in the transient window were reduced. In contrast, subjects with schizophrenia exhibited higher induced 40 Hz power to both stimulus types, consistent with the reduced PLF findings. The method of SSP combined with wavelet based complex demodulation produces a significant improvement in signal-to-noise ratio, and directly estimates the activity of the cortical generators responsible for gamma band auditory MEG evoked fields. Schizophrenic subjects exhibit significant impairment of generation and phase locking of this activity in auditory cortex, suggesting an impairment of GABA-ergic inhibitory interneuronal modulation of pyramidal cell activity.

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“…13,22,24,35,36 However, detailed experimental analyses of the cellular and subcellular mechanisms underlying gamma oscillations have been widely performed in vitro, particularly in neuronal networks of the hippocampus. 16,17,19,37 Rodent hippocampal slices express various patterns of naturally occurring network oscillations and permit high-resolution recordings with electrophysiological methods, live-cell imaging techniques and oxygen sensor microelectrodes under well-defined recording conditions. [38][39][40][41] This in vitro preparation also provides a reasonable model for examining energy metabolism during different forms of neuronal network activation.…”

Section: Gamma Oscillations and Cortical Information Processingmentioning

confidence: 99%

“…70,74,151 In case of inhibitory synapses with dominant Cl À -conductance, restoration of ion gradients is served by secondarily active transporters, especially the K þ /Cl À -cotransporter, KCC2. [16][17][18]144 When chloride enters the cell during synaptic inhibition, subsequent Cl À -transport will be directed outwardly, against the equilibrium potential of chloride. The required driving force for the outward transport is provided by the electrochemical potential of potassium being established by the Na þ /K þ -ATPase.…”

Section: Energy Utilization Of Fast-spiking Behavior and Synaptic Inhmentioning

confidence: 99%

“…In cortical networks, inhibition is mainly mediated by neurotransmitter, g-aminobutyric acid (GABA), and research during the past decade has revealed an astonishing heterogeneity of GABAergic interneurons at the molecular, morphologic and functional level. 16,17 This raises the fundamental question of electrophysiological and neuroenergetical properties of GABAergic interneurons, including the impact on cortical information processing under physiologic conditions as well as pathologic conditions such as ischemia. However, GABAergic interneurons have attracted little attention about brain energy metabolism so far.…”

Section: Introductionmentioning

confidence: 99%

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Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

Kann

Papageorgiou

Draguhn

2014

J Cereb Blood Flow Metab

221

235

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Gamma oscillations (B30 to 100 Hz) provide a fundamental mechanism of information processing during sensory perception, motor behavior, and memory formation by coordination of neuronal activity in networks of the hippocampus and neocortex. We review the cellular mechanisms of gamma oscillations about the underlying neuroenergetics, i.e., high oxygen consumption rate and exquisite sensitivity to metabolic stress during hypoxia or poisoning of mitochondrial oxidative phosphorylation. Gamma oscillations emerge from the precise synaptic interactions of excitatory pyramidal cells and inhibitory GABAergic interneurons. In particular, specialized interneurons such as parvalbumin-positive basket cells generate action potentials at high frequency ('fast-spiking') and synchronize the activity of numerous pyramidal cells by rhythmic inhibition ('clockwork'). As prerequisites, fast-spiking interneurons have unique electrophysiological properties and particularly high energy utilization, which is reflected in the ultrastructure by enrichment with mitochondria and cytochrome c oxidase, most likely needed for extensive membrane ion transport and g-aminobutyric acid metabolism. This supports the hypothesis that highly energized fast-spiking interneurons are a central element for cortical information processing and may be critical for cognitive decline when energy supply becomes limited ('interneuron energy hypothesis'). As a clinical perspective, we discuss the functional consequences of metabolic and oxidative stress in fast-spiking interneurons in aging, ischemia, Alzheimer's disease, and schizophrenia.

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Role of GABAergic inhibition in hippocampal network oscillations

Cited by 350 publications

References 69 publications

GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity

GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity

Cortical source estimates of gamma band amplitude and phase are different in schizophrenia

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

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