Biology of Brain waves: natural history and evolution of an information-rich sign of activity.

Abstract

Using "brain waves" and "EEG" broadly for ongoing electrical activity and stimulus- or event-related activity of organized masses of neural tissue as seen by wideband amplifiers and macro-, micro- or semi-microelectrodes within or in electrical contact with the central nervous system, I consider the character of these signs in animals of many phyla, by various descriptors, emphasizing local field potentials, pregnant questions and research opportunities. We still have inadequate or hardly tested ideas of why most invertebrates, large and small, have inconspicuous slow waves (<50 Hz) and conspicuous spikes. They can, however, show slow waves under certain conditions, somewhat reminiscent of spinal cord, cerebellum or retina. We have even less tested explanations of the strong similarity of all vertebrates: fish, amphibians, reptiles, birds and mammals, large and small - with respect to the power spectrum of conspicuous slow and inconspicuous spikes (until hunted by microelectrodes). Amplitude is the only obvious difference among vertebrate classes, mammals being highest. This may come from an evolution of the prevalence of synchrony, attrubutable, if true, to a generally higher coherence between pairs of sites in reptiles, birds and especially mammals. The strong similarity in the power spectrum, among taxa with and without a cortex, is only one of several reasons to believe that we have not found the most relevant measures to reveal the real structure of the time series, in space and time. Fine structure in the millimeter and fractional second domains, in the seemingly stochastic, wideband component of activity is probably widespread and greater in mammals than in fish. It has properties that are not obvious, such as nonlinear quadratic phase couplings and pseudo-periodicities, locally and episodically. Wavelet analysis, independent component analysis and other tools that might reveal nonrhythmic fine structure have not yet been applied to evolutionary studies. A new tool, the Period-Specific-Average (PSA) can show real rhythms even when the power spectrum does not and shows absence of rhythms at some frequencies where the power spectrum peaks showing Fourier components of irregular transients. The PSA shows that most of the spectrum most of the time in most human cortex is without rhythms. Special conditions bring out episodes of delta, theta, alpha, beta and gamma waves and their subtypes, usually only one or two at once, while most of the energy is wideband and seemingly stochastic. Between episodes of one or two rhythms there are major periods of time in normal human life without any significant rhythm in cortical surface (subdural) and depth electrodes. In spite of many kinds of sophisticated analyses, gross mappings, and models, with our present understanding, we cannot yet anticipate the character of scalp or subdural surface or macroelectrode depth recordings from microelectrode data or vice versa. Also lacking, so far, is any general understanding of the relation of slower, local field potentials and spike firing. Examples are known of strong positive correlations and others show no correlation. Communication among neurons by subthreshold, nonsynaptic routes is probably important in some evolving places and times. The relative neglect of the basic biology, natural history, evolution, and system identification of local field potentials at different scales in different places is undeserved and a prime opportunity for new tools .