Anterior hippocampus and goal-directed spatial decision making

Abstract

Planning spatial paths through our environment is an important part of everyday life and is supported by a neural system including the hippocampus and prefrontal cortex. Here we investigated the precise functional roles of the components of this system in humans by using fMRI as participants performed a simple goal-directed route-planning task. Participants had to choose the shorter of two routes to a goal in a visual scene that might contain a barrier blocking the most direct route, requiring a detour, or might be obscured by a curtain, requiring memory for the scene. The participant's start position was varied to parametrically manipulate their proximity to the goal and the difference in length of the two routes. Activity in medial prefrontal cortex, precuneus, and left posterior parietal cortex was associated with detour planning, regardless of difficulty, whereas activity in parahippocampal gyrus was associated with remembering the spatial layout of the visual scene. Activity in bilateral anterior hippocampal formation showed a strong increase the closer the start position was to the goal, together with medial prefrontal, medial and posterior parietal cortices. Our results are consistent with computational models in which goal proximity is used to guide subsequent navigation and with the association of anterior hippocampal areas with nonspatial functions such as arousal and reward expectancy. They illustrate how spatial and nonspatial functions combine within the anterior hippocampus, and how these functions interact with parahippocampal, parietal, and prefrontal areas in decision making and mnemonic function.

Figure 1.

A, B, Trial structure showing the alternation of encoding phases, in which participants passively view the layout of a room from the middle viewpoint, and test phases, showing the same room from a shifted viewpoint, during which participants had to respond by indicating which gap in the near wall they would go through to get to the man by the shortest possible route (each phase lasted 3 s). Two examples are given with the man shown on the left in the no-detour/memory condition (A) and in the detour/no-memory condition (B). The delay and intertrial intervals (ITI) were both jittered with a mean duration of 4 s.

Figure 2.

A, Aerial view of the layout, shown in the no-detour condition. B, Correspondence between the distance to goal (distances 1–5) and the six start positions (positions 1–6) in the no-detour/no-memory condition, with the shortest route for each start position indicated (participants did not see these routes). In the no-detour condition, the shortest route for start positions 1–5 (red) involved choosing the gap opposite to the man, whereas the shortest route from the sixth start position (green) involved choosing of the gap on the other side. C, Correspondence between distance to goal and start positions in the detour/no-memory condition, with the shortest route for each start position indicated. In the detour condition, the brown gate in the far wall blocks the direct route to the man, so that the goal for the planning task (i.e., the choice of gate in the nearer wall) becomes the other (unblocked) gate in the farther wall. The start positions are organized relative to the goal for the planning task (i.e., number 1 is the closest to the goal in all conditions, but is far from the man in the detour condition).

Figure 3.

A, B, Behavioral results for the detour, memory, and control conditions in terms of performance (i.e., choice of the correct shortest path) (A) and reaction times (B, left). The effect of goal proximity (B, right) (for distance levels, see Fig. 2) on performance and reaction times is shown separately for the detour and memory conditions. Error bars denote SEM. D, Detour; M, memory; NoD, no-detour; NoM, no-memory; ctl, control.

Figure 4.

Statistical parametric maps showing the main results of the factorial analysis. A, Main effect of detour: no-detour versus detour, centered on the right hippocampal peak (x = 26, y = −6, z = −16); detour versus no-detour, centered on the left mPFC peak (Brodmann area 10; x = −18, y = 58, z = −8). B, Main effect of memory: no-memory versus memory, centered on the right inferior occipital peak (Brodmann area 18; x = 30, y = −88, z = −4); memory versus no-memory, centered on the right parahippocampal peak (Brodmann area 36; x = 28, y = −38, z = −18). Stereotaxic coordinates are given in Table 2. Plots show mean percentage signal change of the peak voxel in the indicated region (±SEM) separately for the detour and memory factors. Color scale shows voxel t values. L, Left; R, right.

Figure 5.

Parametric effect of goal proximity. A, B, Left hippocampal (A; x = −26, y = −16, z = −20) and left medial prefrontal (B; x = −2, y = 56, z = −12) activation increases with goal proximity. Statistical parametric maps show the increasing response with increasing proximity to goal (top). Plots show activation (±SEM) for the different levels of proximity to goal (Fig. 2) and control condition (ctl). Stereotaxic coordinates are given in Table 3. Color scale shows voxel t values. For representational purposes, the statistical maps show clusters surviving a height threshold of p < 0.0001.

Figure 6.

Parametric responses of increasing goal distance showing activation in the precuneus (sagittal section), insula (coronal section), and anterior cingulate cortex (both sections). Statistical parametric maps and plots of percentage signal change (±SEM) in the left precuneus (x = 12, y = −58, z = 60) are shown for increasing levels of distance from goal. The farther the start position is from the goal, the higher the activation. Stereotaxic coordinates are given in Table 4. Color scale shows voxel t values.