Rate-specific synchrony: Using noisy oscillations to detect equally active neurons

Abstract

Although gamma frequency oscillations are common in the brain, their functional contributions to neural computation are not understood. Here we report in vitro electrophysiological recordings to evaluate how noisy gamma frequency oscillatory input interacts with the overall activation level of a neuron to determine the precise timing of its action potentials. The experiments were designed to evaluate spike synchrony in a neural circuit architecture in which a population of neurons receives a common noisy gamma oscillatory synaptic drive while the firing rate of each individual neuron is determined by a slowly varying independent input. We demonstrate that similarity of firing rate is a major determinant of synchrony under common noisy oscillatory input: Near coincidence of spikes at similar rates gives way to substantial desynchronization at larger firing rate differences. Analysis of this rate-specific synchrony phenomenon reveals distinct spike timing ''fingerprints'' at different firing rates that emerge through a combination of phase shifting and abrupt changes in spike patterns. We further demonstrate that rate-specific synchrony permits robust detection of rate similarity in a population of neurons through synchronous activation of a postsynaptic neuron, supporting the biological plausibility of a Many Are Equal computation. Our results reveal that spatially coherent noisy oscillations, which are common throughout the brain, can generate previously unknown relationships among neural rate codes, noisy interspike intervals, and precise spike synchrony codes. All of these can coexist in a self-consistent manner because of rate-specific synchrony.gamma oscillations ͉ neural code ͉ neural computation G amma oscillations (30-100 Hz) are observed in field potential recordings from many brain areas (1-4). These oscillations are typically noisy, exhibiting fluctuations in amplitude and a broad frequency distribution. In vitro experiments using cortical brain slices (5) have demonstrated that gamma oscillations can be produced by sustained activation of networks of inhibitory neurons, which in turn produce highly correlated rhythmic membrane potential oscillations in the local population of pyramidal cells (6). This raises the general question of what role common noisy oscillatory synaptic inputs might play in producing synchronous action potentials across a population of neurons with differing mean firing rates. In the presence of correlated noisy gamma, neurons with the same mean firing rate would be expected to produce highly correlated spike trains (7). But what is the level of synchrony that will result when the mean firing rates are different? These correlations would be functionally important because relative spike timing on the millisecond time scale influences synaptic activation of postsynaptic targets (8, 9), timing-dependent short-term synaptic plasticity (10, 11), and pattern recognition (12).Previous work has shown that weakly correlated noisy input to a pair of neurons produces an output correlation p...

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