Theta phase precession of grid and place cell firing in open environments

Abstract

Place and grid cells in the rodent hippocampal formation tend to fire spikes at successively earlier phases relative to the local field potential theta rhythm as the animal runs through the cell's firing field on a linear track. However, this ‘phase precession’ effect is less well characterized during foraging in two-dimensional open field environments. Here, we mapped runs through the firing fields onto a unit circle to pool data from multiple runs. We asked which of seven behavioural and physiological variables show the best circular–linear correlation with the theta phase of spikes from place cells in hippocampal area CA1 and from grid cells from superficial layers of medial entorhinal cortex. The best correlate was the distance to the firing field peak projected onto the animal's current running direction. This was significantly stronger than other correlates, such as instantaneous firing rate and time-in-field, but similar in strength to correlates with other measures of distance travelled through the firing field. Phase precession was stronger in place cells than grid cells overall, and robust phase precession was seen in traversals through firing field peripheries (although somewhat less than in traversals through the centre), consistent with phase coding of displacement along the current direction. This type of phase coding, of place field distance ahead of or behind the animal, may be useful for allowing calculation of goal directions during navigation.

Space in the brain: how the hippocampal formation supports spatial cognition

“…These correlations, and the well-established relationship between theta phase of firing and distance coding in both place cells and grid cells, as further demonstrated by Jeewajee et al in this issue [36], have led to the suggestion that the theta oscillation plays a role in coding for self-motion and can be used to estimate spatial translation [11,37,38]. We consider the phenomenon of phase precession in some detail in §2b(ii) and figure 3, discussing the properties of place cells and grid cells.…”

“…In general, the view that spatial translation might be encoded using the theta oscillation remains influential and controversial. In this special issue, several authors explore this possibility [36,41,42], whereas others take issue with it [43]. Jacobs in this issue [44] considers the possibility that there is a navigation-related oscillation in humans which is homologous to rodent theta, but which occurs at a lower frequency [45,46].…”

Hippocampal Mechanisms for the Segmentation of Space by Goals and Boundaries

“…The synaptic activation causes a time (phase) delay proportional to the distance between the current position and the cell's place field due to greater numbers of intervening cells that must be chained for more distant locations. This type of model places a heavy onus on pre-existing wiring as phase precession can be observed for first time passes through a place field (Feng et al 2015) and in unique trajectories in two-dimensional environments (Harris et al 2002;Huxter et al 2008;Jeewajee et al 2014). These results necessitate pre-existing chains for every running direction for every position, an unlikely scenario.…”

How Animals Find Their Way in Space. Experiments and Modeling

“…Как и для клеток места, для клеток решетки описан эффект фазовой прецессии относительно локального тета-ритма [52]. Более того, при фармакологической блокаде тета-ритма ингибиторами холинергической трансмиссии или при блокаде МСО типичная активность клеток решетки обычно разрушается [53,54] Однако в специфических случаях активность клеток решетки может сохраняться в отсутствие тета-ритма.…”