A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro

Abstract

Basic cellular and network mechanisms underlying gamma frequency oscillations (30 -80 Hz) have been well characterized in the hippocampus and associated structures. In these regions, gamma rhythms are seen as an emergent property of networks of principal cells and fast-spiking interneurons. In contrast, in the neocortex a number of elegant studies have shown that specific types of principal neuron exist that are capable of generating powerful gamma frequency outputs on the basis of their intrinsic conductances alone. These fast rhythmic bursting (FRB) neurons (sometimes referred to as ''chattering'' cells) are activated by sensory stimuli and generate multiple action potentials per gamma period. Here, we demonstrate that FRB neurons may function by providing a large-scale input to an axon plexus consisting of gap-junctionally connected axons from both FRB neurons and their anatomically similar counterparts regular spiking neurons. The resulting network gamma oscillation shares all of the properties of gamma oscillations generated in the hippocampus but with the additional critical dependence on multiple spiking in FRB cells.G amma frequency oscillations are readily recordable from scalp and depth electroencephalogram electrodes placed over or in the neocortex of humans and laboratory animals. They occur spontaneously at low amplitude or transiently at larger amplitudes in response to sensory stimuli (1, 2). Their role in processing of sensory information has been proposed to involve the establishment of a temporal framework within which longrange synchronization of individual neuronal elements coding for specific sensory events can occur (3). Qualitatively similar oscillations also occur in the hippocampus (4) and entorhinal cortex (5), where their generation can be ascribed to the phasic or tonic (or a combination of both) excitation of fast spiking (FS) interneurons, the outputs of which, in turn, provide a temporal framework for controlling the outputs of principal cells (6, 7).Although much is known of the mechanisms underlying gamma oscillations in the archicortex and entorhinal cortex, relatively little evidence is available to suggest a mechanism (or mechanisms) involved in generating neocortical gamma oscillations. What is known is that specific neurons exist within the neocortical mantle that are capable of generating outputs within the gamma frequency range on the basis of intrinsic properties alone (in the absence of influences from local networks). Such neurons exhibit fast rhythmic bursting (FRB), with interburst frequencies of 20 Hz and upward, in response to depolarizing current injection alone (8-10). These FRB neurons (sometimes called ''chattering cells'') have also been shown to participate in visually evoked gamma (25-70 Hz) oscillations in vivo (8), with the FRB cells morphologically identified as spiny layer II͞III pyramidal neurons. Other principal neocortical neurons also possess the ability to generate activity within the gamma band on the basis of intrinsic properties alone in layer IV ...

Intersubject variability and induced gamma in the visual cortex: DCM with empirical Bayes and neural fields

“…Changes in the amplitude of gamma oscillations may be due to interactions between principal cells and interneurons as the grating patch expands beyond the classical receptive field. These interactions are thought to be mediated by local intrinsic (horizontal) connectivity that might drive gamma oscillations [Cunningham et al, 2004; Whittington et al, 1995] and alter their form and coherence [Jia et al, 2013; Ray and Maunsell, 2010]. …”

Temperature- and concentration-dependence of kainate-induced γ oscillation in rat hippocampal slices under submerged condition

“…These oscillations are similar to those recorded in vitro in the entorhinal cortex caused by kainate receptor activation [26] , in vitro in the hippocampus caused by cholinergic activation [6,16,27] and in vivo in the hippocampus [5] but are different from the γ oscillations recorded in the CA1 [14,15,28,29] , which showed that both chemically and electrically interconnected interneuronal networks were involved without any contribution from pyramidal cells. The sodium channel blocker, TTX, also largely reduced γ oscillations, suggesting that neuronal action potentials (spikes) contribute to the network oscillations [30] .…”

A beta2-frequency (20–30 Hz) oscillation in nonsynaptic networks of somatosensory cortex

“…Here, we demonstrate an in vitro model that shows that a beta2 rhythm (20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) can be specifically generated in layer V of neocortex in a manner independent of gamma rhythmogenesis and of glutamatergic synaptic excitation. Beta2 generation in layer V stands in contrast to cortical gamma rhythms that have been shown to originate in layers II͞III in in vitro models (11) and may underlie cortico-cortical synchronization (12).…”