Abstract

Rhythmic voltage oscillations resulting from the summed activity of neuronal populations occur in many nervous systems. Contemporary observations suggest that coexistent oscillations interact and, in time, may switch in dominance. We recently reported an example of these interactions recorded from in vitro preparations of rat somatosensory cortex. We found that following an initial interval of coexistent gamma (∼25 ms period) and beta2 (∼40 ms period) rhythms in the superficial and deep cortical layers, respectively, a transition to a synchronous beta1 (∼65 ms period) rhythm in all cortical layers occurred. We proposed that the switch to beta1 activity resulted from the novel mechanism of period concatenation of the faster rhythms: gamma period (25 ms)+beta2 period (40 ms) = beta1 period (65 ms). In this article, we investigate in greater detail the fundamental mechanisms of the beta1 rhythm. To do so we describe additional in vitro experiments that constrain a biologically realistic, yet simplified, computational model of the activity. We use the model to suggest that the dynamic building blocks (or motifs) of the gamma and beta2 rhythms combine to produce a beta1 oscillation that exhibits cross-frequency interactions. Through the combined approach of in vitro experiments and mathematical modeling we isolate the specific components that promote or destroy each rhythm. We propose that mechanisms vital to establishing the beta1 oscillation include strengthened connections between a population of deep layer intrinsically bursting cells and a transition from antidromic to orthodromic spike generation in these cells. We conclude that neural activity in the superficial and deep cortical layers may temporally combine to generate a slower oscillation.

Highlights

  • The synchronous activity of neural populations results in voltage fluctuations observable in macroscopic and mesoscopic recordings

  • We develop computational models motivated by a novel method of rhythm generation—period concatenation— as we describe

  • Through the combined approach of experimental recordings and mathematical modeling, we identify the cell types, synaptic connections, and ionic currents involved in rhythm generation through period concatenation

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Summary

Introduction

The synchronous activity of neural populations results in voltage fluctuations observable in macroscopic (e.g., scalp electroencephalography) and mesoscopic (e.g., local field potential or LFP) recordings. The purpose of these oscillations remains unknown, neural rhythms appear to temporally organize network activity patterns, and pathological changes in these rhythms often accompany disease [2,3]. Simple characteristic structural patterns appear fundamental to the brain’s organization [5,6]. From these elementary network building blocks (i.e., structural and functional motifs) more complicated structures may be generated in an efficient way [7,8,9]

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