In Vitro Recordings of Human Neocortical Oscillations

Abstract

Electrophysiological oscillations are thought to create temporal windows of communication between brain regions. We show here that human cortical slices maintained in vitro can generate oscillations similar to those observed in vivo. We have characterized these oscillations using local field potential and whole-cell recordings obtained from neocortical slices acquired during epilepsy surgery. We confirmed that such neocortical slices maintain the necessary cellular and circuitry components, and in particular inhibitory mechanisms, to manifest oscillatory activity when exposed to glutamatergic and cholinergic agonists. The generation of oscillations was dependent on intact synaptic activity and muscarinic receptors. Such oscillations differed in electrographic and pharmacological properties from epileptiform activity. Two types of activity, theta oscillations and high gamma activity, uniquely characterized this model-activity not typically observed in animal cortical slices. We observed theta oscillations to be synchronous across cortical laminae suggesting a novel role of theta as a substrate for interlaminar communication. As well, we observed cross-frequency coupling (CFC) between theta phase and high gamma amplitude similar to that observed in vivo. The high gamma "bursts" generated by such CFC varied in their frequency content, suggesting that this variability may underlie the broadband nature of high gamma activity.

Phase–Amplitude Coupling and Interlaminar Synchrony Are Correlated in Human Neocortex

“…Modeling of this metric has revealed that information transfer (transfer entropy) is correlated to the strength of PDPC (Buehlmann and Deco, 2010), suggesting that the coherent theta oscillation we observe here may subserve information transfer between cortical laminae in vivo. Furthermore, axonal delays determine the strength, shape, and optimal frequency at which PDPC is operative (Eriksson et al, 2011), suggesting that a complex bilaminar theta resonant structural circuit motif (Womelsdorf et al, 2014) may underlie our observations. Such interlaminar interactions have been described for alpha oscillations within the occipital lobe (Bollimunta et al, 2008;Spaak et al, 2012), although the analogy to alpha activity in macaque inferotemporal cortex is likely more appropriate given its association with increased multiunit firing rather than inhibition (Mo et al, 2011).…”

Presence of synchrony‐generating hubs in the human epileptic neocortex

“…Furthermore, spontaneous seizure‐like events appeared in neocortical slices derived from epileptic patients, by applying kainate plus carbachol (Florez et al . ), as well as in the Mg 2+ ‐free model (Avoli et al . ; Mattia et al .…”

“…During the course of the seizures, heterogeneous firing patterns were detected in both the human hippocampus (Babb et al 1987) and the neocortex, together with a high ratio of cells increasing their firing rate (Truccolo et al 2011). Furthermore, spontaneous seizure-like events appeared in neocortical slices derived from epileptic patients, by applying kainate plus carbachol (Florez et al 2015), as well as in the Mg 2+ -free model (Avoli et al 1987;Mattia et al 1995), with such seizures being reflected intracellularly as a large depolarizing shift and burst firing (Avoli et al 1997).…”

Neural oscillations in the temporal pole for a temporally congruent audio-visual speech detection task

“…Rhythmic brain activity supports the packaging and segmentation of information, and its coordination across distant brain areas. More recently, brain rhythms at different frequency bands were found to interact with each other2930, a process called “cross-frequency coupling” (CFC) that has attracted increasing interest. One subtype of CFC, phase-amplitude coupling (PAC), has been particularly noteworthy.…”