Asymmetry of the temporal code for space by hippocampal place cells

Abstract

Hippocampal place cells convey spatial information through spike frequency (“rate coding”) and spike timing relative to the theta phase (“temporal coding”). Whether rate and temporal coding are due to independent or related mechanisms has been the subject of wide debate. Here we show that the spike timing of place cells couples to theta phase before major increases in firing rate, anticipating the animal’s entrance into the classical, rate-based place field. In contrast, spikes rapidly decouple from theta as the animal leaves the place field and firing rate decreases. Therefore, temporal coding has strong asymmetry around the place field center. We further show that the dynamics of temporal coding along space evolves in three stages as the animal traverses the place field: phase coupling, sharp precession and phase decoupling. These results suggest that independent mechanisms may govern rate and temporal coding.

Spatial synchronization codes from coupled rate-phase neurons

“…Inset from Fig 1E for illustration. (B) Mean rate-phase relationship across normalized traversals of 1,071 place fields from Souza & Tort (2017) [43]. Arrow: unidirectionality of phase precession.…”

“…Histograms: positive composited over negative; lines: density estimates using a circular π/4 bandwidth Gaussian kernel. Panel (B) was adapted from figure 5B of Souza & Tort (2017) [43] as permitted by the CC-BY 4.0 International License (creativecommons.org/licenses/by/4.0/).…”

“…In contrast, Souza & Tort (2017) [43] examined hippocampal place-cell theta-phase at low firing rates and revealed a distinct angle-shaped rate-phase relationship across place fields. The resulting curve (adapted in Fig 3B) reflects the combination of two effects that progress from entry to exit of hippocampal place fields: (1) the strict unidirectionality of spike theta-phase precession [4], and (2) the single-peaked rise and fall of firing rate, which may be symmetric or skewed with respect to the field center [12, 44].…”

The subiculum: Unique hippocampal hub and more

“…In the hippocampus of freely-behaving animals, the spike timing of place cells progressively advances to earlier phases of extracellular theta cycles as the animal walks through the cell's place field, a phenomenon that is referred to as theta phase precession (O'Keefe and Recce, 1993). The place field and theta phase precession are striking substrates of rate and temporal code of space, respectively, although it is still debated whether the two codes are intrinsically coupled (Harris et al, 2002;Mehta et al, 2002) or definitely independent (Huxter et al, 2003;Souza and Tort, 2017). Subicular principal cells show theta phase precession similar to the CA1 area .…”

Inexpensive, scalable camera system for tracking rats in large spaces

“…An understanding of mechanisms and functions of theta phase precession will benefit from increased accuracy in quantifying theta phase precession. Whereas linear (O’Keefe and Recce 1993) or circular-linear (Huxter et al 2008; Kempter et al 2012) regression is routinely used to quantify theta phase precession, the observed dynamics of theta phase precession are more complex (Mehta et al 2002; Skaggs et al 1996; Souza and Tort 2017; Yamaguchi et al 2002), with the rate of precession changing as a function of location within the place field. Different proposed mechanisms for theta phase precession predict different shape of theta phase precession and variability of the preferred theta phase at different locations within the place field (reviewed in Burgess and O’Keefe 2011).…”