Unconscious relational inference recruits the hippocampus

Abstract

Relational inference denotes the capacity to encode, flexibly retrieve, and integrate multiple memories to combine past experiences to update knowledge and improve decision-making in new situations. Although relational inference is thought to depend on the hippocampus and consciousness, we now show in young, healthy men that it may occur outside consciousness but still recruits the hippocampus. In temporally distinct and unique subliminal episodes, we presented word pairs that either overlapped ("winter-red", "red-computer") or not. Effects of unconscious relational inference emerged in reaction times recorded during unconscious encoding and in the outcome of decisions made 1 min later at test, when participants judged the semantic relatedness of two supraliminal words. These words were either episodically related through a common word ("winter-computer" related through "red") or unrelated. Hippocampal activity increased during the unconscious encoding of overlapping versus nonoverlapping word pairs and during the unconscious retrieval of episodically related versus unrelated words. Furthermore, hippocampal activity during unconscious encoding predicted the outcome of decisions made at test. Hence, unconscious inference may influence decision-making in new situations.

Figure 1.

Presentation procedure for one subliminal episode. Each subliminal word pair was presented twelve times in a 6 s time window, which we call one subliminal episode. Word pairs were flashed for 17 ms flanked by pattern masks that consisted of random arrangements of black and white pixels. A central fixation cross was presented once a second. Once in 6 s (i.e., in one subliminal episode), the fixation cross was replaced by a horizontal or vertical bar. Participants performed an attention task that required them to fixate gaze on the central fixation cross and to indicate by button press the occurrence of a horizontal (left key) and vertical (right key) bar. Figure is reproduced from Reber and Henke (2011).

Figure 2.

Experimental design. Displayed is one of four encoding–retrieval runs. In the encoding part of the run, we presented word pairs subliminally while participants performed an attention task (Fig. 1). In the retrieval part of the run, we presented word pairs with suprathreshold durations for participants to decide whether the two words in a pair fit together semantically or not (“fit”/“don't fit” task). In the encoding and retrieval part of the run, word pairs were grouped by condition into blocks of four word pairs (fMRI block design).

Figure 3.

Behavioral results. The difference in RT on the attention task during blocks of B–C presentations (experimental condition) versus blocks of C–D presentations (control condition) predicted the difference in the number of “fit” responses to A–C pairs (experimental condition) versus A–D pairs (control condition). Top left quadrant, Typical pattern of participants with a convergent style of inference: briefer reaction times to B–C pairs than C–D pairs at encoding and more “fit” answers to A–C than A–D pairs at test. Bottom right quadrant, Typical pattern of participants with a divergent style of inference: longer reaction times to B–C pairs than C–D pairs at encoding and less “fit” answers (or more “don't fit” answers) to A–C than A–D pairs at test.

Figure 4.

Common brain activation in participants with a divergent or convergent style of inference. A, Results in the medial temporal lobe of a conjunction analysis performed on the encoding contrasts (B–C > C–D) of convergent and divergent thinkers. B, Results in the medial temporal lobe of a conjunction analysis performed on the retrieval contrasts (A–C > A–D) of convergent and divergent thinkers. A, B, Commonly activated regions are depicted in yellow and reach significance at a height threshold of p = 0.001 (uncorrected) and an extent threshold of 0 voxel. These fMRI results are presented on sagittal sections of a T1-weighted MNI template of SPM. L, Left; R, right.

Figure 5.

Encoding activity predicted performance at test. Results of the correlation between the encoding contrast (B–C > C–D) and the absolute difference in the number of “fit” responses given to A–C (experimental condition) versus A–D pairs (control condition) at test. Because we used absolute difference values in this correlation, high test scores represent a good performance in both convergent and divergent thinkers. Significant results of the correlation are depicted in yellow and marked by a blue crosshair on coronal sections of a T1-weighted MNI template of SPM. These results reached significance at a height threshold of p = 0.001 (uncorrected) and an extent threshold of 0 voxel for medial temporal lobe areas and 20 voxels for all other brain regions. Significant correlations are also presented in scatter plots, where blue symbols stand for convergent thinkers and red symbols for divergent thinkers. The first eigenvariate of a significant cluster was extracted and depicted in arbitrary units on the y-axes of the scatter plots. L, Left; R, right.