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

Abstract

Objective: To explain the neural mechanisms of spontaneous EEG by measuring the spatiotemporal patterns of synchrony among beta–gamma oscillations during perception. Methods: EEGs were measured from 8×8 (5.6×5.6 mm 2) arrays fixed on the surfaces of primary sensory areas in rabbits that were trained to discriminate visual, auditory or tactile conditioned stimuli (CSs) eliciting conditioned responses (CRs). EEG preprocessing was by (i) bandpass filtering to extract the beta-gamma range (deleting theta-alpha); (ii) low-pass spatial filtering (not high-pass Laplacians used for localization), (iii) spatial averaging (not time averaging used for evoked potentials), and (iv) close spacing of 64 electrodes for simultaneous recording in each area (not sampling single signals from several areas); (v) novel algorithms were devised to measure synchrony and spatial pattern stability by calculating variances among patterns in 64-space derived from the 8×8 arrays (not by fitting equivalent dipoles). These methodological differences are crucial for the proposed new perspective on EEG. Results: Spatial patterns of beta–gamma EEG emerged following sudden jumps in cortical activity called ‘state transitions’. Each transition began with an abrupt phase re-setting to a new value on every channel, followed sequentially by re-synchronization, spatial pattern stabilization, and a dramatic increase in pattern amplitude. State transitions recurred at varying intervals in the theta range. A novel parameter was devised to estimate the perceptual information in the beta-gamma EEG, which disclosed 2–4 patterns with high information content in the CS–CR interval on each trial; each began with a state transition and lasted ∼0.1 s. Conclusions: The function of each primary sensory neocortex was discontinuous; discrete spatial patterns occurred in frames like those in cinema. The frames before and after the CS–CR interval had low content. Significance: Derivation and interpretation of unit data in studies of perception might benefit from using multichannel EEG recordings to define distinctive epochs that are demarcated by state transitions of neocortical dynamics in the CS–CR intervals, particularly in consideration of the possibility that EEG may reveal recurring episodes of exchange and sharing of perceptual information among multiple sensory cortices. Simultaneously recorded, multichannel beta-gamma EEG might assist in the interpretation of images derived by fMRI, since high beta–gamma EEG amplitudes imply high rates of energy utilization. The spatial pattern intermittency provides a tag to distinguish gamma bursts from contaminating EMG activity in scalp recording in order to establish beta–gamma recording as a standard clinical tool. Finally, EEG cannot fail to have a major impact on brain theory.