Signals and signs in the nervous system: The dynamic anatomy of electrical activity is probably information-rich

Signals and signs in the nervous system: The dynamic anatomy of electrical activity is probably information-rich

Theodore Holmes Bullock

Department of Neurosciences, University of California at San Diego, La Jolla, CA 92093-0201

Abstract

The dichotomy between two groups of workers on neuroelectrical activity is retarding progress. To study the interrelations between neuronal unit spike activity and compound field potentials of cell populations is both unfashionable and technically challenging. Neither of the mutual disparagements is justified: that spikes are to higher functions as the alphabet is to Shakespeare and that slow field potentials are irrelevant epiphenomena. Spikes are not the basis of the neural code but of multiple codes that coexist with nonspike codes. Field potentials are mainly information-rich signs of underlying processes, but sometimes they are also signals for neighboring cells, that is, they exert influence. This paper concerns opportunities for new research with many channels of wide-band (spike and slow wave) recording. A wealth of structure in time and three-dimensional space is different at each scale—micro-, meso-, and macroactivity. The depth of our ignorance is emphasized to underline the opportunities for uncovering new principles. We cannot currently estimate the relative importance of spikes and synaptic communication vs. extrasynaptic graded signals. In spite of a preponderance of literature on the former, we must consider the latter as probably important. We are in a primitive stage of looking at the time series of wide-band voltages in the compound, local field, potentials and of choosing descriptors that discriminate appropriately among brain loci, states (functions), stages (ontogeny, senescence), and taxa (evolution). This is not surprising, since the brains in higher species are surely the most complex systems known. They must be the greatest reservoir of new discoveries in nature. The complexity should not deter us, but a dose of humility can stimulate the flow of imaginative juices.

Footnotes

Abbreviations: EEG, electroencephalogram; EP, evoked potential; ERP, event-related potential; LFP, local field potential.
↵ * Notable exceptions go back to Adrian, Jasper, and others, cited in ref. 1; a modern one is ref. 2.
↵ † The scattered literature on extrasynaptic influences, including the effects of slow field potentials, is partially represented in ref. 3 and on the following pages of ref. 4: 14–19, 20–24, 46–53, 97–111, 116–123, and 545–568.
↵ ‡ I must admit another motivation. This is a plea that spike workers take a bit of extra trouble to control power-line interference and insert impedance changers close to the preparation so that the filters can be opened to record a wide-band channel. Their valuable data can then be correlated with slow potentials—by others if they are not themselves so moved. This would be a significant contribution toward bridging the gulf between knowledge of spikes and slow potentials—far beyond simply sharing animals.
↵ § Coherence is a pairwise estimate that measures the fraction of the energy in each frequency that maintains a fixed phase (of whatever value) between the two time series, throughout the sample epoch. It is normalized for power and gives a value between 0 and 1.0 for each frequency. The method of choice for measuring the synchrony in a population, this has been studied in a few species of mammals, including humans, a few reptiles, fish, and invertebrates, based on multichannel recording from regularly spaced electrodes on the pial surface or within the brain (16–18). Average coherence is found to fall to 0.5 in 7–10 mm on the pia mater in humans, 4–6 mm in rat and rabbit, 2–3 mm in gecko and turtle, ≈2 mm in elasmobranchs, and <0.5 mm in the neuropil of the gastropod Aplysia. The variation around these means is greater for recordings within the neuropil than on the surface.
↵ ¶ In terms of literature, the major part of this category concerns the scalp-recorded EEG and evoked or event-related potentials, commonly read from ≈20 electrodes at ≈4-cm spacing, but in some laboratories with closer spacing and upwards of 120 electrodes. The effect of observing through the skin and skull is mainly spatial smoothing by looking at a large cone of brain; this tends to reduce the recorded amplitude and the relative strength of higher frequencies, although the skin and skull are not considered to be serious frequency filters (19).
↵ ‖ These terms are often used today, not for a rhythm or wave visible above the wide-band background, or in their specific historic sense which included the brain state, but simply as shorthand to designate a frequency band, for example the alpha or 8- to 12-Hz band, even in white noise. This is a form of jargon, convenient for the writer but much less preferable for the reader than stating the numbers.