Rhythm Generation through Period Concatenation in Rat Somatosensory Cortex

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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. Since the late 19th century, rhythmic electrical activity has been observed in the mammalian brain. Although subject to intense scrutiny, only a handful of these rhythms are understood in terms of the biophysical elements that produce the oscillations. Even less understood are the mechanisms that underlie interactions between rhythms; how do rhythms of different frequencies coexist and affect one another in the dynamic environment of the brain? In this article, we consider a recent proposal for a novel mechanism of cortical rhythm generation: period concatenation, in which the periods of faster rhythms sum to produce a slower oscillation. To model this phenomenon, we implement simple—yet biophysical—computational models of the individual neurons that produce the brain's voltage activity. We utilize established models for the faster rhythms, and unite these in a particular way to generate a slower oscillation. Through the combined approach of experimental recordings (from thin sections of rat cortex) and mathematical modeling, we identify the cell types, synaptic connections, and ionic currents involved in rhythm generation through period concatenation. In this way the brain may generate new activity through the combination of preexisting elements.