Signals and signs in the nervous system: The dynamic anatomy of electrical activity

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 also signals for neighboring cells, that is, exert influence. This paper concerns opportunities for new research with many channels of wideband (spike and slow wave) recording. A wealth of structure in time and 3-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 wideband 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 imaginative juices.