Verbal Paired Associates and the Hippocampus: The Role of Scenes

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). Resolving the tension among hippocampal theories concerning the VPA could be important for leveraging a fuller understanding of hippocampal function. Notably, VPA tasks typically use high imagery concrete words and so conflate imagery and binding. To determine why VPA engages the hippocampus, we devised an fMRI encoding task involving closely matched pairs of scene words, pairs of object words, and pairs of very low imagery abstract words. We found that the anterior hippocampus was engaged during processing of both scene and object word pairs in comparison to abstract word pairs, despite binding occurring in all conditions. This was also the case when just subsequently remembered stimuli were considered. Moreover, for object word pairs, fMRI activity patterns in 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. This may help to resolve the issue that visuospatial hippocampal theories have in accounting for verbal memory.

Figure 1.. Example stimuli and trial timeline. (A) Examples of stimuli from each of the word types in the order of (from left to right) Scene word pair, Object word pair, and Abstract word pair. (B) Examples of single word trials in the order of (from left to right) Scene single word, Object single word, and Abstract single word. Single words were shown with random letter strings (which could be presented at either the top or the bottom) to be similar to the visual presentation of the word pairs. (C) Examples of catch trials, where a real word was presented with a pseudoword, which could be presented as either the top or bottom word. (D) Example timeline of several trials.

Figure 2.. Memory performance on the associative memory test shown by percentage correct (left) and d′ (right). Error bars are 1 SEM. ^ indicates a significant difference from chance (for percentage correct the dashed line indicates chance at 50%, for d′ it is 0) at p < .001. Stars show the significant differences across the word pair types: **p < .01, ***p < .001.

Figure 3.. Comparison of high imagery Scene or Object word pairs with very low imagery Abstract word pairs. The sagittal slice is of the left hemisphere, which is from the ch2better template brain in MRicron (Rorden & Brett, ; Holmes et al., 1998). The left of the image is the left side of the brain. The colored bar indicates the t value associated with each voxel. (A) Scene word pairs > Abstract word pairs. (B) Object word pairs > Abstract word pairs. Images are thresholded at p < .001 uncorrected for display purposes.

Figure 4.. Brain areas more activated by Scene word pairs than Object word pairs. The sagittal slice is of the left hemisphere, which is from the ch2better template brain in MRicron (Rorden & Brett, ; Holmes et al., 1998). The left of the image is the left side of the brain. The colored bar indicates the t value associated with each voxel. Images are thresholded at p < .001 uncorrected for display purposes.

Figure 5.. Comparison of each word pair condition with a fixation cross baseline. Mean beta values extracted from a bilateral anatomical mask of the anterior hippocampus for each of the word pair conditions compared with the central fixation cross baseline. Error bars are 1 SEM. A repeated-measures ANOVA showed significant differences between the conditions, F(1.69, 74.51) = 16.06, p < .001, η² = .27. Follow-up paired t tests revealed significant differences between Scene word pairs versus Abstract word pairs, t(44) = 6.46, p < .001, d_rm = 0.70; Scene word pairs versus Object word pairs, t(44) = 2.97, p = .005, d_rm = 0.30; Object word pairs versus Abstract word pairs, t(44) = 2.51, p = .016, d_rm = 0.34. *p < .05, **p < .01, ***p < .001.

Figure 6.. The neural similarity of Object word pairs, Scene single words, and Object single words separately for the anterior and posterior hippocampus. (A) Anterior hippocampus. (B) Posterior hippocampus. Object Pair Object Pair = the similarity between Object word pairs between runs; Object Pair Scene Single = the similarity between Object word pairs and Scene single words; Object Pair Object Single = the similarity between Object word pairs and Object single words. Error bars represent 1 SEM adjusted for repeated-measures (Morey, 2008). *p < .05.

Figure 7.. RSA comparisons of the three imagery groups separately for the anterior and posterior hippocampus. (A) The neural similarity of Object word pairs, Scene single words, and Object single words in the anterior hippocampus when split by self-reported imagery use. Object Pair Scene Single = the similarity between Object word pairs and Scene single words; Object Pair Object Single = the similarity between Object word pairs and Object single words. (B) The difference in similarity between Object word pairs and Scene single words compared with Object words pairs and Object single words in the imagery groups in the anterior hippocampus. (C) The neural similarity of Object word pairs, Scene single words, and Object single words in the posterior hippocampus when split by self-reported imagery use. Object Pair Scene Single = the similarity between Object word pairs and Scene single words; Object Pair Object Single = the similarity between Object word pairs and Object single words. (D) The difference in similarity between Object word pairs and Scene single words compared with Object words pairs and Object single words in the imagery groups in the posterior hippocampus. Error bars represent 1 SEM. *p < .05, ***p < .001.