Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons

Abstract

Intracellular recording and computational modelling suggest that interactions of subthreshold membrane potential oscillation frequency in different dendritic branches of entorhinal cortex stellate cells could underlie the functional coding of continuous dimensions of space and time. Among other things, these interactions could underlie properties of grid cell field spacing. The relationship between experimental data on membrane potential oscillation frequency (f) and grid cell field spacing (G) indicates a constant scaling factor H=fG. This constant scaling factor between temporal oscillation frequency and spatial periodicity provides a starting constraint that is used to derive the model of Burgess, Barry and O'Keefe (Hippocampus, in press). This model provides a consistent quantitative link between single cell physiological properties and properties of spiking units in awake behaving animals. Further properties and predictions of this model about single cell and network physiological properties are analyzed. In particular, the model makes quantitative predictions about the change in membrane potential, single cell oscillation frequency and network oscillation frequency associated with speed of movement, about the independence of single cell properties from network theta rhythm oscillations, and about the effect of variations in initial oscillatory phase on the pattern of grid cell firing fields. These same mechanisms of subthreshold oscillations may play a more general role in memory function, by providing a method for learning arbitrary time intervals in memory sequences.

Towards a functional organization of the medial temporal lobe memory system: Role of the parahippocampal and medial entorhinal cortical areas

“…The observation of spatial firing patterns in the MEC encouraged us to ask whether the disambiguation of places on the maze by temporal context occurred within the hippocampus or instead occurred earlier in the cortical-hippocampal hierarchy, specifically in the MEC. This possibility is consistent with the suggestion that sequences are bound by a shared temporal context signal that may exist in the entorhinal area (Hasselmo and Eichenbaum, 2005;Hasselmo et al, 2007;Hasselmo, 2007; see also Hasselmo, 2008).…”

“…Our speculative interpretation that MEC neuronal firing patterns contain a signal for temporal context is based on the observation that MEC spatial firing often extended through a substantial distance on the maze, and these firing patterns varied as a function of trial type. The connection between these two properties may be that sustained firing patterns serve as the neural bridge that links sequential events subsequently identified within the hippocampus, and does so differentially for each trial type (Hasselmo and Eichenbaum, 2005;Hasselmo et al, 2007;Hasselmo, 2007; see also Hasselmo, 2008). In this way, MEC activity that spans multiple spatial locations signals what is common about those locations in terms of an animal's ongoing behavior, that is, a leftvs.…”

The role of ongoing dendritic oscillations in single-neuron dynamics

“…A recent model for the grid field properties of the entorhinal cortex layer II stellate cells [22,23,38] relies precisely on the ingredients considered in the present study. The model assumes that different dendritic branches emanating from the soma of these cells function as distinct oscillators.…”

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

“…This model provides an alternate implementation of the oscillatory interference model Burgess, 2008) that is compared to the implementation using membrane potential oscillations Hasselmo et al, 2007;Giocomo and Hasselmo, 2008a).…”

“…Previous modeling showed that membrane potential oscillations in entorhinal neurons might also contribute to grid cell firing Giocomo et al, 2007;Hasselmo et al, 2007;Giocomo and Hasselmo, 2008a). Entorhinal Layer II stellate cells show subthreshold membrane potential oscillations when depolarized near firing threshold (Alonso and Llinas, 1989;Alonso and Klink, 1993;Giocomo et al, 2007).…”