A mechanism for generation of long-range synchronous fast oscillations in the cortex

Abstract

Synchronous neuronal oscillations in the 30-70 Hz range, known as gamma oscillations, occur in the cortex of many species. This synchronization can occur over large distances, and in some cases over multiple cortical areas and in both hemispheres; it has been proposed to underlie the binding of several features into a single perceptual entity. The mechanism by which coherent oscillations are generated remains unclear, because they often show zero or near-zero phase lags over long distances, whereas much greater phase lags would be expected from the slow speed of axonal conduction. We have previously shown that interneuron networks alone can generate gamma oscillations; here we propose a simple model to explain how an interconnected chain of such networks can generate coherent oscillations. The model incorporates known properties of excitatory pyramidal cells and inhibitory interneurons; it predicts that when excitation of interneurons reaches a level sufficient to induce pairs of spikes in rapid succession (spike doublets), the network will generate gamma oscillations that are synchronized on a millisecond time-scale from one end of the chain to the other. We show that in rat hippocampal slices interneurons do indeed fire spike doublets under conditions in which gamma oscillations are synchronized over several millimetres, whereas they fire single spikes under other conditions. Thus, known properties of neurons and local synaptic circuits can account for tightly synchronized oscillations in large neuronal ensembles.

Cognitive dysfunction in schizophrenia: unifying basic research and clinical aspects

“…Gamma range (30 to 50 Hz) neural synchronization may be a key mechanism of information processing in neural networks, underlying the binding of both sensory and temporal features of objects. Furthermore gamma range synchronization is thought to depend on the glutamatergically mediated interplay between excitatory projection neurons and GABAergic circuits (see Traub et al 1996), which we have postulated to be abnormal. We thus have obtained preliminary data on synchronization in response to auditory input (McCarley et al, in press).…”

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

“…12 Dominant patterns in cortical networks comprise theta-(4 to 12 Hz), beta-(13 to 30 Hz) and gamma-(B30 to 100 Hz) frequency oscillations, which synchronize the action potential generation ('spiking') of principal cells with great precision, sometimes over large distances of corticocortical connections. 10,[13][14][15] Importantly, inhibitory interneurons have a key role in organizing these highly coordinated patterns of activity. 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.…”

Origin, structure, and role of background EEG activity. Part 1. Analytic amplitude

“…The same currents are largely responsible for local field potentials and EEG. The firing is grouped in time by oscillations in dendritic current in the beta (12-30 Hz) and gamma (30-80 Hz) ranges that arise from negative feedback among excitatory and inhibitory neurons (Freeman, 1975(Freeman, , 2004; Appendix 2.4 in Part 2) with facilitation by the molecular dynamics of synaptic receptors (Traub et al, 1996;Whittington et al, 2000;Kopell et al, 2000). The synchrony between pairs of EEG records can be measured by any of a variety of methods (Lachaux et al, 1999;Le Van Quyen et al, 2001;Quiroga et al, 2002), including the phase difference of oscillations in which they share the same frequency.…”