Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms

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Abstract

Despite the several-thousand-fold increase of brain volume during the course of mammalian evolution, the hierarchy of brain oscillations remains remarkably preserved, allowing for multiple-time-scale communication within and across neuronal networks at approximately the same speed, irrespective of brain size. Deployment of large-diameter axons of long-range neurons could be a key factor in the preserved time management in growing brains. We discuss the consequences of such preserved network constellation in mental disease, drug discovery, and interventional therapies.

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Page 752

This in turn provides windows of alternating reduced and enhanced excitability (Bishop, 1933; Lindsley, 1952) and offers natural temporal frames for grouping, or ‘‘chunking,’’ neuronal activity into cell assemblies and sequences of assemblies for the effective exchange of information among cortical networks (Destexhe and Sejnowski, 2003; Wilson and McNaughton, 1994; Steriade et al., 1993a; Fries, 2005; Buzsa ́ ki, 2010).

Page 752

Integrated over a long temporal scale, the power distribution of the various frequencies has the appearance of 1/fn ‘‘noise’’ (Nunez, 1981), partly reflecting the fact that slow oscillations generate large, synchronous membrane-potential fluctuations in many neurons in brain-wide networks (He et al., 2008), whereas faster oscillations are associated with smaller changes in membrane potential in a limited number of cells, that are synchronized only within a restricted neural volume (Figure 1B).

Page 752

The nature of interaction is usually hierarchical and universal, so that the phase of the slower oscillation modulates the power of the faster ones (Figure 1B; Bragin et al., 1995; Chrobak and Buzsa ́ ki, 1998; Leopold et al., 2003; Schroeder and Lakatos, 2009; Canolty et al., 2006; Buzsa ́ ki and Wang, 2012; Fell and Axmacher, 2011).