Abstract
It is widely agreed that patients with bilateral hippocampal damage are impaired at binding pairs of words together. Consequently, the verbal paired associates (VPA) task has become emblematic of hippocampal function. This VPA deficit is not well understood, and is particularly difficult for hippocampal theories with a visuospatial bias to explain (e.g., cognitive map and scene construction theories). Notably, however, VPA tasks typically use concrete imageable words and so conflate imagery and binding. To determine why VPA engages the hippocampus, we devised an fMRI encoding task involving pairs of scene words, pairs of object words and pairs of non-imageable abstract words which were closely matched on a wide range of features. Using univariate and multivariate methods we found that the anterior hippocampus in particular was engaged during the encoding of both scene and object word pairs. This was not the case for abstract word pairs, despite binding occurring here also, and even when only subsequently-remembered trials were considered. Moreover, for object word pairs, fMRI activity patterns in the anterior hippocampus were more similar to those for scene imagery than object imagery. This was especially evident in participants who were high imagery users, and not in mid and low imagery users. Overall, our results show that hippocampal engagement during VPA, even when object word pairs are involved, seems to be evoked by scene imagery rather than binding per se. This may help to resolve the issue that visuospatial hippocampal theories have in accounting for verbal memory.
Significance Statement Binding pairs of words together is a task closely associated with the hippocampus. Therefore, explaining exactly how it achieves this could be important for leveraging a fuller understanding of hippocampal function. To date, word pair tasks have confounded the binding process with the use of words that are easy to imagine. We devised a task that separated binding from imagery. Combining this with functional MRI brain scanning we found that engagement of the anterior hippocampus was associated with imageability, and in particular the use of scene imagery, rather than binding. Moreover, this was especially true for participants who were high imagery users. We conclude that even apparently verbal tasks may be processed by the hippocampus by means of scene imagery.
Footnotes
The authors declare no competing financial interests and no conflicts of interest.