Selective entrainment of gamma subbands by different slow network oscillations

• Published in: Proceedings of the National Academy of Sciences - PNAS 2017-04, Vol.114 (17), p.4519-4524
• Main Authors: Zhong, Weiwei, Ciatipis, Mareva, Wolfenstetter, Thérèse, Jessberger, Jakob, Müller, Carola, Ponsel, Simon, Yanovsky, Yevgenij, Brankačk, Jurij, Tort, Adriano B. L., Draguhn, Andreas
• Format: Article
• Language: English
• Subjects: Activity patterns; Biological Sciences; Brain; Cortex (olfactory); Cortex (parietal); Coupling; Data processing; Entrainment; Exploration; Hippocampus; Information processing; Mice; Neural coding; Neurons; Olfactory bulb; Oscillations; Respiration; Rhythm; Rodents; Switching theory; Temporal lobe; Theta rhythms
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1617249114

Theta oscillations (4–12 Hz) are thought to provide a common temporal reference for the exchange of information among distant brain networks. On the other hand, faster gamma-frequency oscillations (30–160 Hz) nested within theta cycles are believed to underlie local information processing. Whether oscillatory coupling between global and local oscillations, as showcased by theta-gamma coupling, is a general coding mechanism remains unknown. Here, we investigated two different patterns of oscillatory network activity, theta and respiration-induced network rhythms, in four brain regions of freely moving mice: olfactory bulb (OB), prelimbic cortex (PLC), parietal cortex (PAC), and dorsal hippocampus [cornu ammonis 1 (CA1)]. We report differential state- and region-specific coupling between the slow large-scale rhythms and superimposed fast oscillations. During awake immobility, all four regions displayed a respiration-entrained rhythm (RR) with decreasing power from OB to CA1, which coupled exclusively to the 80- to 120-Hz gamma subband (γ₂). During exploration, when theta activity was prevailing, OB and PLC still showed exclusive coupling of RR with γ₂ and no theta-gamma coupling, whereas PAC and CA1 switched to selective coupling of theta with 40- to 80-Hz (γ₁) and 120- to 160-Hz (γ₃) gamma subbands. Our data illustrate a strong, specific interaction between neuronal activity patterns and respiration. Moreover, our results suggest that the coupling between slow and fast oscillations is a general brain mechanism not limited to the theta rhythm.