Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies

Abstract

Hebb proposed that neuronal cell assemblies are critical for effective perception, cognition, and action. However, evidence for brain mechanisms that coordinate multiple coactive assemblies remains lacking. Neuronal oscillations have been suggested as one possible mechanism for cell assembly coordination. Prior studies have shown that spike timing depends upon local field potential (LFP) phase proximal to the cell body, but few studies have examined the dependence of spiking on distal LFP phases in other brain areas far from the neuron or the influence of LFP-LFP phase coupling between distal areas on spiking. We investigated these interactions by recording LFPs and single-unit activity using multiple microelectrode arrays in several brain areas and then used a unique probabilistic multivariate phase distribution to model the dependence of spike timing on the full pattern of proximal LFP phases, distal LFP phases, and LFP-LFP phase coupling between electrodes. Here we show that spiking activity in single neurons and neuronal ensembles depends on dynamic patterns of oscillatory phase coupling between multiple brain areas, in addition to the effects of proximal LFP phase. Neurons that prefer similar patterns of phase coupling exhibit similar changes in spike rates, whereas neurons with different preferences show divergent responses, providing a basic mechanism to bind different neurons together into coordinated cell assemblies. Surprisingly, phasecoupling-based rate correlations are independent of interneuron distance. Phase-coupling preferences correlate with behavior and neural function and remain stable over multiple days. These findings suggest that neuronal oscillations enable selective and dynamic control of distributed functional cell assemblies.neuronal oscillations | neuronal ensembles | spike timing | local field potentials | brain rhythms S ignificant progress has been made in understanding the dynamics and response properties of single nerve cells (1, 2) and how they interconnect to form cortical microcircuits (3, 4). More than 60 y ago, however, Donald Hebb hypothesized that the fundamental unit of brain operation is not the single neuron but rather the cell assembly-an anatomically dispersed but functionally integrated ensemble of neurons (5). The individual neurons that compose an assembly may reside in widely separated brain areas but act as a single functional unit through coordinated network activity. Dynamic interactions between multiple assemblies may then give rise to the large-scale functional networks found in mammalian brains (6-8). Despite the theoretical appeal of Hebb's idea (9) and growing empirical evidence of assemblies (10-12), it remains unclear how diverse groups of neurons spanning several cortical regions transiently coordinate their activity to form cell assemblies or how multiple coactive assemblies regulate their interactions to form larger functional networks.Brain rhythms may play a key role in coordinating neuronal ensembles (13-15), with a dynamic hierarchy of neuronal osc...

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