Imagination as a fundamental function of the hippocampus

Abstract

Imagination is a biological function that is vital to human experience and advanced cognition. Despite this importance, it remains unknown how imagination is realized in the brain. Substantial research focusing on the hippocampus, a brain structure traditionally linked to memory, indicates that firing patterns in spatially tuned neurons can represent previous and upcoming paths in space. This work has generally been interpreted under standard views that the hippocampus implements cognitive abilities primarily related to actual experience, whether in the past (e.g. recollection, consolidation), present (e.g. spatial mapping) or future (e.g. planning). However, relatively recent findings in rodents identify robust patterns of hippocampal firing corresponding to a variety of alternatives to actual experience, in many cases without overt reference to the past, present or future. Given these findings, and others on hippocampal contributions to human imagination, we suggest that a fundamental function of the hippocampus is to generate a wealth of hypothetical experiences and thoughts. Under this view, traditional accounts of hippocampal function in episodic memory and spatial navigation can be understood as particular applications of a more general system for imagination. This view also suggests that the hippocampus contributes to a wider range of cognitive abilities than previously thought. This article is part of the theme issue 'Thinking about possibilities: mechanisms, ontogeny, functions and phylogeny'.

Keywords: hippocampus; imagination; memory; place cells; replay; theta.

Figure 1.

Hippocampal neural firing patterns schematic. (a) Place cell firing. Left: a rat runs on a linear maze. Middle: the firing activity of multiple neurons is recorded simultaneously from the hippocampus while the rat runs. Right: one example recorded place cell fires in the same spatial location on the track over many runs, but with notable variability across individual runs (firing denoted by raster lines). The time-averaged firing of the example place cell over many runs forms the cell's place field (oval). (b) Generative place cell firing examples. Left: place field locations (ovals) of multiple place cells (A–F) that fire as the rat runs along the linear maze (one run takes approx. 2 s). Right: examples (ex 1–4) of generative firing patterns that occur when the rat is not actually in the cells' place field locations. Place cell firing is denoted by cell-coloured raster lines. Ex 1: replay occurs while sleeping in an environment separate from the maze. Ex 2: replay occurs while rat is stationary at the lower maze end. Ex 3: replay occurs while rat is stationary and in a different maze environment (light grey lines indicate firing of a cell active in the different maze, but not active on the maze shown at Left). Ex 4: occurs while the rat is running on the maze, during the theta rhythm. In ex 1–4, place cell firing corresponds to a series of locations not presently occupied by the rat. (Online version in colour.)

Figure 2.

Generative activity corresponding to alternative possibilities. (a) Example of neural firing corresponding to alternative locations. Left: a rat running on the central arm of a bifurcating maze can either turn left or right. Middle: individual place cells fire when the animal is in particular place field locations on the maze (ovals coloured by cell). Right: generative activity. While the rat is resting at the end of the central maze arm, generative neural firing during a sharp wave-ripple (SWR) can replay other locations (raster lines coloured by cell). At other times while the rat is running up the central maze arm towards the bifurcation, neural firing during the theta rhythm alternates between current and upcoming locations within each cycle, and between the left and right trajectories ahead across the second halves of theta cycles. (b) Example of neural firing corresponding to alternative directions. Left: a rat on a linear maze can run in up or down directions. Middle: different sets of direction-selective place cells fire in their place field locations (ovals) when the rat runs up or down (ovals coloured by cell). Right: generative activity. Neural firing during SWRs replays locations that do not correspond to the rat's actual location at the end of the maze. Additionally, while the rat is running in one direction, cells corresponding to the rat's actual (red) and alternative (blue) directions fire in alternation along the theta rhythm. (Online version in colour.)

Figure 3.

Two views of hippocampal firing during network-level activity patterns. (a) Generative view (proposed). Neural firing during early theta phases represents actual circumstances, while representations during late theta phases and sharp wave-ripple (SWR) replays are imagined (generative). (b) Episodic view (traditional). Neural firing during each theta cycle corresponds to sequential locations in the past, present and future, and neural firing during SWR replays correspond to past or future locations. Note that the episodic view can be understood as a particular application of the proposed generative view. (Online version in colour.)

Figure 4.

Schema for interpreting hippocampal activity. We suggest that generative activity arising from the hippocampus may not only correspond to the experienced past or anticipated future, but also to a wide range of possibilities. This view may also organize or suggest various cognitive functions.