Spatial synchronization codes from coupled rate-phase neurons

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.

Cognitive swarming in complex environments with attractor dynamics and oscillatory computing

“…While the phenomenon is less clear in open, 2-dimensional environments, phase precession has been observed in particular traversals of the firing fields of place cells as well as grid cells in entorhinal cortex (Climer et al, 2013;Jeewajee et al, 2014). However, our analysis of phaser cells in the lateral septum (Monaco et al, 2019a) revealed a more direct phase code for 2-dimensional position that was consistent with a minimal model of temporal phase-coding ( Fig. 1C).…”

“…A weakness of the presented implementation was the use of a global, shared oscillation without allowing for noise, drift, or independent perturbations (cf. Zilli and Hasselmo, 2010;Monaco et al, , 2019a. A more decentralized approach might utilize resonant agent-oscillators that self-organize local oscillations depending on available information, task requirements, or context.…”

“…The resulting 'phase precession,' a monotonic advance in timing from late to early within each theta cycle, may enhance the precision and temporal organization of spatial codes (O'Keefe and Recce, 1993;Jensen and Lisman, 2000;Foster and Wilson, 2007;Drieu et al, 2018) in ways that support decisionmaking and/or deliberative planning during subsequent sleep or quiescent states (Buzsáki, 1989;Johnson and Redish, 2007;Buzsáki and Moser, 2013;Wikenheiser and Redish, 2015;Papale et al, 2016;Muessig et al, 2019). Recently, in contrast to phase precession, we discovered a novel class of spatial phase-coding neurons in open field environments termed 'phaser cells' that were located predominantly in the rat lateral septum and characterized by a strong coupling of theta-phase timing to firing rates (Monaco et al, 2019a). This coupling supports an intrinsic neuronal mechanism of phase-coding that may theoretically transform spatial information to synchronize downstream targets using the global theta oscillation (Monaco et al, 2019a).…”

“…C. Schematic of a minimal model of temporal-phase coding in which an excitatory external input (green) is rhthmically modulated by a continuous inhibitory oscillation (blue) such as the hippocampal theta rhythm. Adapted from Monaco et al (2019a) as permitted by the CC-BY 4.0 International License (creativecommons.org/licenses/by/4.0/).…”

Identifying Core Regions for Path Integration on Medial Entorhinal Cortex of Hippocampal Formation

“…Another review article on the similarities and differences in the hippocampus between rodents and primates [48] was important research but was excluded in this paper to focus on rodents. An article on "phaser cells" and their simulation [49] was also excluded because phaser cells were discovered mainly in the medial septum that is related to the hippocampus. As a result, three articles [50][51][52] were left out of 11 papers.…”