Arc length coding by interference of theta frequency oscillations may underlie context-dependent hippocampal unit data and episodic memory function

Abstract

Many memory models focus on encoding of sequences by excitatory recurrent synapses in region CA3 of the hippocampus. However, data and modeling suggest an alternate mechanism for encoding of sequences in which interference between theta frequency oscillations encodes the position within a sequence based on spatial arc length or time. Arc length can be coded by an oscillatory interference model that accounts for many features of the context-dependent firing properties of hippocampal neurons observed during performance of spatial memory tasks. In continuous spatial alternation, many neurons fire selectively depending on the direction of prior or future response (left or right). In contrast, in delayed non-match to position, most neurons fire selectively for task phase (sample vs. choice), with less selectivity for left versus right. These seemingly disparate results are effectively simulated by the same model, based on mechanisms similar to a model of grid cell firing in entorhinal cortex. The model also simulates forward shifting of firing over trials. Adding effects of persistent firing with reset at reward locations addresses changes in context-dependent firing with different task designs. Arc length coding could contribute to episodic encoding of trajectories as sequences of states and actions.Many models of the hippocampus focus on strengthening of synaptic connections between neurons to encode associations between sequential patterns of neural activity representing items or locations (McNaughton and

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.…”

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

“…Note that though the reward is presented at different locations, the phase is reset to the same zero vector. In contrast to a previous paper about the arc length model (Hasselmo, 2007), these simulations use input from speed-modulated head direction cells (the Euclidian model) rather than using one-dimensional speed input. Also, the simulations presented here include separate populations of entorhinal neurons and hippocampal neurons and address two additional tasks: spatial alternation with running in a wheel during delay (Pastalkova and Buzsaki, 2007;Pastalkova et al, 2008), and the hairpin maze task (Derdikman et al, 2006).…”

“…Reset results in separate twodimensional maps for different phases of a task. In an alternative model, referred to here as the arc length model, the phase of spiking or oscillation can be shifted by running speed alone, independent of head direction (Hasselmo, 2007). In this case, the integration of speed by phase results in firing dependent upon the one-dimensional arc length of a trajectory (Hasselmo, 2007).…”

“…The possibility of reset was mentioned in the original oscillatory interference model presentation , but there is a further division of models based on the mechanism of phase update (Hasselmo, 2007). In the original Euclidian model, a two-dimensional representation of space results from phase integration of input from speed-modulated head direction cells.…”