Coordinating different representations in the hippocampus

Abstract

The processes that organize different thoughts and memories, allowing the separation of currently relevant and irrelevant information, are collectively known as cognitive control. The neuronal mechanisms of these processes can be investigated by place cell ensemble recordings during behaviors and environmental manipulations that present cognitive control challenges to selectively represent one of multiple possible alternative estimates of location. We review place cell studies that investigate responses to manipulations that dissociate the environment into two or more spatial frames of locations, often times to test notions of pattern separation. Manipulations, such as continuously rotating the recording chamber reveal that the ensemble discharge in hippocampus self-organizes into multiple, transiently-organized representations of space, each defined by the subset of coactive cells. Ensemble discharge in the hippocampus alternates between separate representations of frame-specific positions on timescales from 25 ms to several seconds. The dynamic, functional grouping of discharge into transiently co-active subsets of cells is predicted by the animal's changing behavioral needs. In addition to identifying neural correlates of cognitive control in hippocampus, these observations demonstrate that the separation of neuronal activity into distinctive representations depends on ongoing cognitive demands and that what can appear as noise, deviations from receptive field tuning, can substantially be the result of these internal knowledge-guided fluctuations. These findings inspire a new perspective that should be taken into account when investigating pattern separation--a perspective that emphasizes changes in hippocampal neural discharge that are happening on a short timescale and does not assume that patterns of neural discharge are steady and stationary across the several minutes of the recordings.

Viewpoints: how the hippocampus contributes to memory, navigation and cognition

“…24 for review). Furthermore, in tasks in which decisions depend on knowing one's position relative to a shifting goal, rodents are only able to find the goal or avoid the shock when the spatial representation in hippocampus is aligned to that goal's coordinate system 49,50 . An interesting question is whether hippocampus is necessary for deliberative, planning actions.…”

Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus

“…There is rather large heterogeneity of place cell behaviors: some place cells “globally remap” (i.e., gain or lose place fields at given locations) while other place cells “rate remap” (i.e., maintain place field location but have consistently different firing rates under the different conditions). Moreover, rate remapping is not simply a long‐term average of an all‐or‐none firing phenomenon with a rate that depends on condition (Figure ), as would be expected if there were multiple maps that were being switched between, one in which the cell has a place field at that location and others in which it does not (Jackson & Redish, ; Kelemen & Fenton, ; Olypher et al, ). Rather, we show that even when restricting analysis to theta cycles on which a cell is active and therefore in the appropriate map, there are still firing rate changes between the conditions.…”

“…Interestingly, one theory that has been proposed to explain this excess variability provides an alternative interpretation of rate remapping. It has been shown that, for a task in which an animal must switch between maze and room cues, there are actually separate hippocampal maps for the two reference frames and the hippocampus switches between them in a task‐dependent way (Fenton et al, ; Kelemen & Fenton, ). It has been suggested that this process of map switching may actually be a more general phenomenon that occurs under all conditions and that the hippocampus switches between maps at a frequency of 1–10 Hz (Olypher, L'ansky, & Fenton, ; Jackson & Redish, ; Jezek, Henriksen, Treves, Moser, & Moser, ).…”

Three brain states in the hippocampus and cortex

“…One clue is that map switching can occur as fast as at the subsecond timescale (Harris et al, ; Jackson & Redish, ; Jezek et al, ; Kelemen & Fenton, ; Kelemen & Fenton, ) and is thus temporally flexible enough to support a rapidly evolving ongoing behavioral need. It has been argued before that the interlinking of multiple maps through switching allows for flexible recall of similar experiences for the sake of effective problem solving, particularly in circumstances requiring inference (e.g., goal‐directed navigation; Cohen & Eichenbaum, ; Eichenbaum et al, ; Eichenbaum & Cohen, ).…”