Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation

Gulyás, Attila I.; Freund, T.

doi:10.1016/j.conb.2014.07.020

Cited by 69 publications

(55 citation statements)

References 76 publications

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“…How do the experimental observations fit with circuit models of ripple oscillations (Cutsuridis and Taxidis, 2013, Buzsaki, 2015, Gulyas and Freund, 2015, Patel, 2015)? Three main classes of models of ripple oscillations have been proposed, each making different predictions regarding the types of input CA1 pyramidal neurons receive.…”

Section: Discussionmentioning

confidence: 99%

Membrane Potential Dynamics of CA1 Pyramidal Neurons during Hippocampal Ripples in Awake Mice

Hulse

Moreaux

Lubenov

et al. 2016

Neuron

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Ripples are high-frequency oscillations associated with population bursts in area CA1 of the hippocampus that play a prominent role in theories of memory consolidation. While spiking during ripples has been extensively studied, our understanding of the subthreshold behavior of hippocampal neurons during these events remains incomplete. Here, we combine in vivo whole-cell and multisite extracellular recordings to characterize the membrane potential dynamics of identified CA1 pyramidal neurons during ripples. We find that the subthreshold depolarization during ripples is uncorrelated with the net excitatory input to CA1, while the post-ripple hyperpolarization varies proportionately. This clarifies the circuit mechanism keeping most neurons silent during ripples. On a finer time scale, the phase delay between intracellular and extracellular ripple oscillations varies systematically with membrane potential. Such smoothly varying delays are inconsistent with models of intracellular ripple generation involving perisomatic inhibition alone. Instead, they suggest that ripple-frequency excitation leading inhibition shapes intracellular ripple oscillations.

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Section: Discussionmentioning

confidence: 99%

Membrane Potential Dynamics of CA1 Pyramidal Neurons during Hippocampal Ripples in Awake Mice

Hulse

Moreaux

Lubenov

et al. 2016

Neuron

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“…Distinguishing normal physiological HFO (nHFO) [37–41,48 ▪▪ ] from pathological, epileptiform HFO (pHFO) [34,35,36,51] remains a fundamental challenge in clinical epileptology [52 ▪▪ ,53,54 ▪▪ ,55 ▪ ]. Classic examples of physiological and pathological HFOs are ripple frequency oscillations [37,38].…”

Section: Introductionmentioning

confidence: 99%

“…Classic examples of physiological and pathological HFOs are ripple frequency oscillations [37,38]. The sharp–wave–ripple complex is a physiological HFO that results from phasic inhibitory input on the soma of pyramidal cells [56]; whereas the ripple and fast ripple oscillations superimposed on interictal epileptiform sharp waves are largely generated by synchronized pyramidal cell burst firing [54 ▪▪ ,55 ▪ ]. Although currently it is unclear how to definitively differentiate pHFO from nHFO in clinical iEEG recordings, one approach is to simply classify HFO associated with epileptiform sharp waves as pHFO and event-related HFO associated with physiological tasks as nHFO [35,40].…”

Section: Introductionmentioning

confidence: 99%

Interictal high-frequency oscillations in focal human epilepsy

Cimbálník¹,

Kucewicz

Worrell³

2016

Current Opinion in Neurology

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Purpose of review Localization of focal epileptic brain is critical for successful epilepsy surgery and focal brain stimulation. Despite significant progress, roughly half of all patients undergoing focal surgical resection, and most patients receiving focal electrical stimulation, are not seizure free. There is intense interest in high-frequency oscillations (HFOs) recorded with intracranial electroencephalography as potential biomarkers to improve epileptogenic brain localization, resective surgery, and focal electrical stimulation. The present review examines the evidence that HFOs are clinically useful biomarkers. Recent findings Performing the PubMed search ‘High-Frequency Oscillations and Epilepsy’ for 2013–2015 identifies 308 articles exploring HFO characteristics, physiological significance, and potential clinical applications. Summary There is strong evidence that HFOs are spatially associated with epileptic brain. There remain, however, significant challenges for clinical translation of HFOs as epileptogenic brain biomarkers: Differentiating true HFO from the high-frequency power changes associated with increased neuronal firing and bandpass filtering sharp transients. Distinguishing pathological HFO from normal physiological HFO. Classifying tissue under individual electrodes as normal or pathological. Sharing data and algorithms so research results can be reproduced across laboratories. Multicenter prospective trials to provide definitive evidence of clinical utility.

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“…Much less is currently known about dendritic integrative processes in interneurons, although some results do suggest that their dendrites may also have non-linear properties and may have roles beyond the faithful transmission of synaptically evoked signals to the axosomatic output region (Saraga et al, 2003; Chiovini et al, 2014). Meanwhile, a set of studies examined the interactions of specific cell types in cortical networks, with the aim of understanding the generation of different kinds of population dynamics such as coherent oscillations and transient synchrony (Butler and Paulsen, 2015; Gulyás and Freund, 2015). These studies employed somatic patch-clamp recordings and extracellular electrode arrays in vivo and in vitro (Ylinen et al, 1995; Lakatos et al, 2005; Mann et al, 2005; Oren et al, 2006, 2010; Montgomery et al, 2009; Makarov et al, 2010; Sullivan et al, 2011; Scheffer-Teixeira et al, 2012, 2013), which allow recording from all layers of a structure and the calculation of currents flowing in and out of neurons during different activity patterns.…”

Section: Introductionmentioning

confidence: 99%

The Effects of Realistic Synaptic Distribution and 3D Geometry on Signal Integration and Extracellular Field Generation of Hippocampal Pyramidal Cells and Inhibitory Neurons

Gulyás

Freund

Káli

2016

Front. Neural Circuits

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In vivo and in vitro multichannel field and somatic intracellular recordings are frequently used to study mechanisms of network pattern generation. When interpreting these data, neurons are often implicitly considered as electrotonically compact cylinders with a homogeneous distribution of excitatory and inhibitory inputs. However, the actual distributions of dendritic length, diameter, and the densities of excitatory and inhibitory input are non-uniform and cell type-specific. We first review quantitative data on the dendritic structure and synaptic input and output distribution of pyramidal cells (PCs) and interneurons in the hippocampal CA1 area. Second, using multicompartmental passive models of four different types of neurons, we quantitatively explore the effect of differences in dendritic structure and synaptic distribution on the errors and biases of voltage clamp measurements of inhibitory and excitatory postsynaptic currents. Finally, using the 3-dimensional distribution of dendrites and synaptic inputs we calculate how different inhibitory and excitatory inputs contribute to the generation of local field potential in the hippocampus. We analyze these effects at different realistic background activity levels as synaptic bombardment influences neuronal conductance and thus the propagation of signals in the dendritic tree. We conclude that, since dendrites are electrotonically long and entangled in 3D, somatic intracellular and field potential recordings miss the majority of dendritic events in some cell types, and thus overemphasize the importance of perisomatic inhibitory inputs and belittle the importance of complex dendritic processing. Modeling results also suggest that PCs and inhibitory neurons probably use different input integration strategies. In PCs, second- and higher-order thin dendrites are relatively well-isolated from each other, which may support branch-specific local processing as suggested by studies of active dendritic integration. In the electrotonically compact parvalbumin- and cholecystokinincontaining interneurons, synaptic events are visible in the whole dendritic arbor, and thus the entire dendritic tree may form a single integrative element. Calretinin-containing interneurons were found to be electrotonically extended, which suggests the possibility of complex dendritic processing in this cell type. Our results also highlight the need for the integration of methods that allow the measurement of dendritic processes into studies of synaptic interactions and dynamics in neural networks.

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Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation

Cited by 69 publications

References 76 publications

Membrane Potential Dynamics of CA1 Pyramidal Neurons during Hippocampal Ripples in Awake Mice

Membrane Potential Dynamics of CA1 Pyramidal Neurons during Hippocampal Ripples in Awake Mice

Interictal high-frequency oscillations in focal human epilepsy

The Effects of Realistic Synaptic Distribution and 3D Geometry on Signal Integration and Extracellular Field Generation of Hippocampal Pyramidal Cells and Inhibitory Neurons

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