An FMRI analysis of the human hippocampus: inference, context, and task awareness

Abstract

The hippocampus is critical for encoding and retrieving semantic and episodic memories. Animal studies indicate that the hippocampus is also required for relational learning tasks. A prototypical relational learning task, and the one investigated in this experiment, using event-related functional magnetic resonance imaging, is the transitive inference (TI) task. In the TI task, participants were to choose between A and B (A?B) and learned by trial and error to choose A (A > B). There were four such premise pairs during a training (A > B, B > C, C > D, D > E). These can be acquired distinctly or can be organized into a superordinate hierarchy (A > B > C > D > E), which would efficiently represent all the learned relations and allow inferences (e.g., B > D). At test there was no reinforcement: In addition to premise pairs, untrained pairings were introduced (e.g., A?E, B?D). Correctly inferring that B > D is taken as evidence for the formation of a superordinate hierarchy; several alternatives to the superordinate hierarchy hypothesis are considered. Awareness of the formation of this hierarchy was measured by a postscan questionnaire. Four main findings are reported: (1) Inferential performance and task awareness dissociated behaviorally and at the level of hemodynamic response; (2) As expected, performance on the inferred relation, B > D, corresponded to the ability to simultaneously acquire B > C and C > D premise pairs during training; (3) Interestingly, acquiring these "inner pairs" corresponded to greater hippocampal activation than the "outer pairs" (A > B, D > E) for all participants. However, a distinct pattern of hippocampal activity for these inner pairs differentiated those able to perform the inferential discrimination, B > D, at test. Because these inner premise pairs require contextual discrimination (e.g., C is incorrect in the context of B but correct in the context of D), we argue that the TI task is hippocampal-dependent because the premise pair acquisition necessary for inference is hippocampal-dependent; (4) We found B > D related hippocampal activity at test that is anatomically consistent with preconsolidation recall effects shown in other studies.

Figure 1

An example of the five Hiragana characters used as stimuli in the TI task.

Figure 2

Behavioral results: accuracy during training (A) and test (B) as a function of pair type and block number. Frequency distribution of awareness scores (C).

Figure 3

Mean accuracy on the BD pair as a function of trial presentation number. Coordinates (Talairach & Tournoux, 1988), in brackets, are the center of mass for the active region.

Figure 4

Training activation by pair type (inner vs. outer) over time in the left hippocampus and accompanying AUC graph. Coordinates (Talairach & Tournoux, 1988), in brackets, are the center of mass for the active region.

Figure 5

Test activation for B?D pair presentation over all participants and accompanying AUC graph. Coordinates (Talairach & Tournoux, 1988), in brackets, are the center of mass for the active region.

Figure 6

Performance-dependent training interaction contrast: The interaction of inner and outer pairs by time over levels of performance in the left hippocampus. The simplified AUC graph displays activation to the outer pairs subtracted from the inner pairs. Coordinates (Talairach & Tournoux, 1988), in brackets, are the center of mass for the active region.

Figure 7

Activation during the B?D pair at test related to both performance and awareness. Coordinates (Talairach & Tournoux, 1988), in brackets, are the center of mass for the active region.