The hippocampal CA3 region can generate two distinct types of sharp wave‐ripple complexes, in vitro

Hofer, Katharina T.; Kandrács, Ágnes; Ulbert, István; Pál, Ildikó; Szabó, Csilla; Héja, László; Wittner, Lúcia

doi:10.1002/hipo.22361

Cited by 21 publications

(15 citation statements)

References 47 publications

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“…Some SPW-R subtypes reported in the present work are in agreement with recently reported SPW-R signatures in slice models (32,33). However, Hofer et al (32) report only two event classes based on the SPW polarity in CA3.…”

Section: Discussionsupporting

confidence: 93%

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Diversity of sharp-wave–ripple LFP signatures reveals differentiated brain-wide dynamical events

Ramírez-Villegas

Logothetis

Besserve

2015

Proc. Natl. Acad. Sci. U.S.A.

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Sharp-wave-ripple (SPW-R) complexes are believed to mediate memory reactivation, transfer, and consolidation. However, their underlying neuronal dynamics at multiple scales remains poorly understood. Using concurrent hippocampal local field potential (LFP) recordings and functional MRI (fMRI), we study local changes in neuronal activity during SPW-R episodes and their brain-wide correlates. Analysis of the temporal alignment between SPW and ripple components reveals well-differentiated SPW-R subtypes in the CA1 LFP. SPW-R-triggered fMRI maps show that ripples aligned to the positive peak of their SPWs have enhanced neocortical metabolic up-regulation. In contrast, ripples occurring at the trough of their SPWs relate to weaker neocortical up-regulation and absent subcortical down-regulation, indicating differentiated involvement of neuromodulatory pathways in the ripple phenomenon mediated by long-range interactions. To our knowledge, this study provides the first evidence for the existence of SPW-R subtypes with differentiated CA1 activity and metabolic correlates in related brain areas, possibly serving different memory functions.hippocampus | memory | in vivo electrophysiology | fMRI | local field potential M emory processes require mechanisms for large-scale integration of neuronal activity, in which information processing is precisely coordinated at multiple scales. A prominent example of such phenomenon is the replay of specific sequences of action potentials of hippocampal and neocortical neurons, reflecting previous experiences during wakefulness (1-7). Sharpwave-ripple (SPW-R) complexes observed in the hippocampal CA1 local field potential (LFP) mark the reactivation of these sequences by the simultaneous occurrence of two distinct but related phenomena: a strong LFP deflection, known as sharp wave (SPW), and a high-frequency oscillation known as ripple (8,9). SPW-R episodes are thought to reflect brain-wide processes mediating memory consolidation (10-13). However, the largescale cooperative mechanisms associated to these episodes and their relationship to the observed SPW-R electrical signature remain largely unknown. Investigating this relationship is critical for understanding memory processes at a system level and may provide new insights into the mechanisms of pathological fast ripples observed during epilepsy (14).Although they were initially thought to occur during slow-wave sleep and quiescence periods, later on SPW-R and sequence replay were also observed during or shortly after active behavior (15-17). Moreover, many SPW-Rs occur at path choice points (18,19), which are also locations where vicarious trial and error are reported (20). Thus, reactivation of memory sequences during SPW-Rs could provide a convenient mechanism not only for consolidation of long-term memory (4) but also for quickly recalling memories during awake state, serving various cognitive functions (21). The generation of SPW-R complexes in these various contexts likely involves brain-wide network mechanisms, and as a conseq...

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Section: Discussionsupporting

confidence: 93%

“…However, Hofer et al (32) report only two event classes based on the SPW polarity in CA3. In contrast, Reichinnek et al (33) have also observed two SPW-R event classes, differing only in SPW amplitude.…”

Section: Discussionmentioning

confidence: 99%

Diversity of sharp-wave–ripple LFP signatures reveals differentiated brain-wide dynamical events

Ramírez-Villegas

Logothetis

Besserve

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Interestingly, a similar observation was made in rodent hippocampal slices (Hofer et al, 2014) where microspikes or synchronized discharges were interpreted as normal phenomena of the cortex.…”

Section: Micro-spike/macro-spikesupporting

confidence: 63%

Intracranial neuronal ensemble recordings and analysis in epilepsy

Tóth

Fabó

Entz

et al. 2016

Journal of Neuroscience Methods

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Pathological neuronal firing was demonstrated 50 years ago as the hallmark of epileptically transformed cortex with the use of implanted microelectrodes. Since then, microelectrodes remained only experimental tools in humans to detect unitary neuronal activity to reveal physiological and pathological brain functions. This recording technique has evolved substantially in the past few decades; however, based on recent human data implying their usefulness as diagnostic tools, we expect a substantial increase in the development of microelectrodes in the near future.Here, we review the technological background and history of microelectrode array development for human examinations in epilepsy, including discussions on of wire-based and microelectrode arrays fabricated using micro-electro-mechanical system (MEMS) techniques and novel future techniques to record neuronal ensemble.We give an overview of clinical and surgical considerations, and try to provide a list of probes on the market with their availability for human recording. 2Then finally, we briefly review the literature on modulation of single neuron for the treatment of epilepsy, and highlight the current topics under examination that can be background for the future development.3

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“…A relationship between the recurrence frequency and the field potential amplitude has been previously observed in cases of population events in vitro (Papatheodoropoulos & Kostopoulos, ; Hofer et al . ), i.e. as the frequency of events increases as a consequence of higher levels of [K + ] o , the field potential amplitude decreases.…”

Section: Resultsmentioning

confidence: 99%

Hyperexcitability of the network contributes to synchronization processes in the human epileptic neocortex

Tóth

Hofer

Kandrács

et al. 2017

The Journal of Physiology

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Interictal activity is a hallmark of epilepsy diagnostics and is linked to neuronal hypersynchrony. Little is known about perturbations in human epileptic neocortical microcircuits, and their role in generating pathological synchronies. To explore hyperexcitability of the human epileptic network, and its contribution to convulsive activity, we investigated an in vitro model of synchronous burst activity spontaneously occurring in postoperative tissue slices derived from patients with or without preoperative clinical and electrographic manifestations of epileptic activity. Human neocortical slices generated two types of synchronies. Interictal-like discharges (classified as epileptiform events) emerged only in epileptic samples, and were hypersynchronous bursts characterized by considerably elevated levels of excitation. Synchronous population activity was initiated in both epileptic and non-epileptic tissue, with a significantly lower degree of excitability and synchrony, and could not be linked to epilepsy. However, in pharmacoresistant epileptic tissue, a higher percentage of slices exhibited population activity, with higher local field potential gradient amplitudes. More intracellularly recorded neurons received depolarizing synaptic potentials, discharging more reliably during the events. Light and electron microscopic examinations showed slightly lower neuron densities and higher densities of excitatory synapses in the human epileptic neocortex. Our data suggest that human neocortical microcircuits retain their functionality and plasticity in vitro, and can generate two significantly different synchronies. We propose that population bursts might not be pathological events while interictal-like discharges may reflect the epileptogenicity of the human cortex. Our results show that hyperexcitability characterizes the human epileptic neocortical network, and that it is closely related to the emergence of synchronies.

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The hippocampal CA3 region can generate two distinct types of sharp wave‐ripple complexes, in vitro

Cited by 21 publications

References 47 publications

Diversity of sharp-wave–ripple LFP signatures reveals differentiated brain-wide dynamical events

Diversity of sharp-wave–ripple LFP signatures reveals differentiated brain-wide dynamical events

Intracranial neuronal ensemble recordings and analysis in epilepsy

Hyperexcitability of the network contributes to synchronization processes in the human epileptic neocortex

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