Spatial synchronization codes from coupled rate-phase neurons.

Joseph D Monaco,Rose M De Guzman,Kechen Zhang,Hugh T Blair,Daniel Bush

doi:10.1371/journal.pcbi.1006741

Abstract

During spatial navigation, the frequency and timing of spikes from spatial neurons including place cells in hippocampus and grid cells in medial entorhinal cortex are temporally organized by continuous theta oscillations (6–11 Hz). The theta rhythm is regulated by subcortical structures including the medial septum, but it is unclear how spatial information from place cells may reciprocally organize subcortical theta-rhythmic activity. Here we recorded single-unit spiking from a constellation of subcortical and hippocampal sites to study spatial modulation of rhythmic spike timing in rats freely exploring an open environment. Our analysis revealed a novel class of neurons that we termed ‘phaser cells,’ characterized by a symmetric coupling between firing rate and spike theta-phase. Phaser cells encoded space by assigning distinct phases to allocentric isocontour levels of each cell’s spatial firing pattern. In our dataset, phaser cells were predominantly located in the lateral septum, but also the hippocampus, anteroventral thalamus, lateral hypothalamus, and nucleus accumbens. Unlike the unidirectional late-to-early phase precession of place cells, bidirectional phase modulation acted to return phaser cells to the same theta-phase along a given spatial isocontour, including cells that characteristically shifted to later phases at higher firing rates. Our dynamical models of intrinsic theta-bursting neurons demonstrated that experience-independent temporal coding mechanisms can qualitatively explain (1) the spatial rate-phase relationships of phaser cells and (2) the observed temporal segregation of phaser cells according to phase-shift direction. In open-field phaser cell simulations, competitive learning embedded phase-code entrainment maps into the weights of downstream targets, including path integration networks. Bayesian phase decoding revealed error correction capable of resetting path integration at subsecond timescales. Our findings suggest that phaser cells may instantiate a subcortical theta-rhythmic loop of spatial feedback. We outline a framework in which location-dependent synchrony reconciles internal idiothetic processes with the allothetic reference points of sensory experience.

Highlights

A prominent temporal code of neural activity [1,2,3] is the phase precession of rodent place cell and grid cell activity relative to the septal-hippocampal theta rhythm (6–11 Hz) [4, 5], in which firing begins late in the theta cycle and advances to earlier phases as the animal moves across a spatial firing field
We found a class of lateral septum (LS) and hippocampal neurons with 2D spatial phase codes for which we analyzed the relationship between rate and phase, stability of rate and phase coding, temporal organization by theta, spatial firing patterns, and spatial vs. trajectory-related selectivity
By setting criteria for spatial phase coding, we analyzed a subset of these neurons that we termed ‘phaser cells’ to reveal how spatial information was carried in the phase alignment of firing with the hippocampal theta oscillation observed in local field potentials (LFPs)

Summary

Introduction

A prominent temporal code of neural activity [1,2,3] is the phase precession of rodent place cell and grid cell activity relative to the septal-hippocampal theta rhythm (6–11 Hz) [4, 5], in which firing begins late in the theta cycle and advances to earlier phases as the animal moves across a spatial firing field. Theta-phase precession is strictly unidirectional, which ensures that phase unambiguously encodes the distance traveled through a place field [6] This unidirectionality may follow from mechanisms such as neuronal adaptation that halts firing before the peak of dendritic excitation [7], place-cell network plasticity that learns an asymmetric ramp of depolarizing input through experience [8], or temporal interference between a somatic theta oscillation and a speed-tuned [4, 9] or spatial [7, 10,11,12] dendritic oscillation. In open-field foraging, these mechanisms may lock the phase-distance code of phase precession to trajectory details (that is, the speed, running direction, and path) of individual passes through a spatial firing field [13, 14], preventing a direct mapping of phase to spatial locations. Organizing VCOs into ring attractor networks provides some internal stability [26, 27], but biological variance in spike timing and local theta cycle periods limits the temporal precision of VCO phase computations [28, 29]

Methods

Results

Discussion

Conclusion