Affiliation:
1. McKnight Brain Institute, Department of Neuroscience, University of Florida, Gainesville, Florida
2. Engineering School of Sustainable Infrastructure and Environment, University of Florida, Gainesville, Florida
3. Institute of Aging, University of Florida, Gainesville, Florida
4. Department of Biomedical Engineering, University of Florida, Gainesville, Florida
Abstract
Oscillations in the hippocampal local field potential at theta and gamma frequencies are prominent during awake behavior and have demonstrated several behavioral correlates. Both oscillations have been observed to increase in amplitude and frequency as a function of running speed. Previous investigations, however, have examined the relationship between speed and each of these oscillation bands separately. Based on energy cascade models where “…perturbations of slow frequencies cause a cascade of energy dissipation at all frequency scales” (Buzsaki G. Rhythms of the Brain, 2006), we hypothesized that cross-frequency interactions between theta and gamma should increase as a function of speed. We examined these relationships across multiple layers of the CA1 subregion, which correspond to synaptic zones receiving different afferents. Across layers, we found a reliable correlation between the power of theta and the power of gamma, indicative of an amplitude-amplitude relationship. Moreover, there was an increase in the coherence between the power of gamma and the phase of theta, demonstrating increased phase-amplitude coupling with speed. Finally, at higher velocities, phase entrainment between theta and gamma increases. These results have important implications and provide new insights regarding how theta and gamma are integrated for neuronal circuit dynamics, with coupling strength determined by the excitatory drive within the hippocampus. Specifically, rather than arguing that different frequencies can be attributed to different psychological processes, we contend that cognitive processes occur across multiple frequency bands simultaneously with organization occurring as a function of the amount of energy iteratively propagated through the brain. NEW & NOTEWORTHY Often, the theta and gamma oscillations in the hippocampus have been believed to be a consequence of two marginally overlapping phenomena. This perspective, however, runs counter to an alternative hypothesis in which a slow-frequency, high-amplitude oscillation provides energy that cascades into higher frequency, lower amplitude oscillations. We found that as running speed increases, all measures of cross-frequency theta-gamma coupling intensify, providing evidence in favor of the energy cascade hypothesis.
Funder
HHS | NIH | National Institute of Mental Health (NIMH)
Evelyn F. McKnight Brain Research Foundation (McKnight Brain Research Foundation)
Diversity Supplement
Publisher
American Physiological Society
Subject
Physiology,General Neuroscience
Cited by
35 articles.
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