Modeling of grid cell activity demonstrates in vivo entorhinal ‘look-ahead’ properties

Abstract

Recent in vivo data show ensemble activity in medial entorhinal neurons that demonstrates ‘look-ahead’ activity, decoding spatially to reward locations ahead of a rat deliberating at a choice point while performing a cued, appetitive T-Maze task. To model this experiment's look-ahead results, we adapted previous work that produced a model where scans along equally probable directions activated place cells, associated reward cells, grid cells, and persistent spiking cells along those trajectories. Such look-ahead activity may be a function of animals performing scans to reduce ambiguity while making decisions. In our updated model, look-ahead scans at the choice point can activate goal-associated reward and place cells, which indicate the direction the virtual rat should turn at the choice point. Hebbian associations between stimulus and reward cell layers are learned during training trials, and the reward and place layers are then used during testing to retrieve goal-associated cells based on cue presentation. This system creates representations of location and associated reward information based on only two inputs of heading and speed information which activate grid cell and place cell layers. We present spatial and temporal decoding of grid cell ensembles as rats are tested with perfect and imperfect stimuli. Here, the virtual rat reliably learns goal locations through training sessions and performs both biased and unbiased look-ahead scans at the choice point. Spatial and temporal decoding of simulated medial entorhinal activity indicates that ensembles are representing forward reward locations when the animal deliberates at the choice point, emulating in vivo results.

Hippocampal theta sequences reflect current goals

“…PFC neural activity shows consistent organization relative to hippocampal theta 43,44 , coherence in the local field potential at theta frequency increases between these structures during decision-making 45 , and theta entrainment of PFC spiking predicts accurate behavioral performance 46 . Prospective hippocampal representations of upcoming spatial locations could facilitate decision-related information processing in these and other brain regions to adaptively guide behavior 47,48 . Pyramidal neurons in a range of brain regions are known to be exquisitely sensitive to temporally patterned dendritic inputs 49,50 , suggesting a possible mechanism by which cells receiving hippocampal inputs could detect even subtle differences in the content of theta sequence representations.…”

A High‐resolution study of hippocampal and medial temporal lobe correlates of spatial context and prospective overlapping route memory

“…This localization of entorhinal activity may be significant because the posterior entorhinal cortex of primates has similar connectivity to the medial entorhinal cortex of rodents (Suzuki and Amarai, ; van Strien et al, ). The medial entorhinal cortex of rodents contains grid cells which are theorized to be particularly important for spatial memory and may be important for disambiguation processes (Hafting et al, ; Lipton et al, ; Moser and Moser, ; Moser et al, ; Hasselmo, ; Gupta et al, , in press). In humans, the entorhinal cortex has been implicated in learning (Schon et al, ; Suthana et al, ).…”

Neuronal Computation Underlying Inferential Reasoning in Humans and Mice

“…We next investigated the hippocampal computation that serves inference. In the spatial domain, spiking activity in the medial temporal lobe can sweep ahead of an animal's location (Gupta et al, 2013;Johnson and Redish, 2007;Mehta et al, 2000) and predict subsequent behavior (Ferbinteanu and Shapiro, 2003;Pastalkova et al, 2008;Pfeiffer and Foster, 2013;Singer et al, 2013;Wood et al, 2000). We reasoned that if similar predictive activity serves inferential choice in the cognitive domain, the hippocampus should draw on mnemonic relationships to prospectively represent visual cues Yn in response to auditory cues Xn in the inference test, thereby chaining Xn to outcome Zn.…”