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Contributor Information. This article has been cited by other articles in PMC. 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.

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.

But one point on which there is general agreement is that people with bilateral hippocampal damage and concomitant amnesia hippocampal amnesia are significantly impaired on verbal paired associates VPA tasks. Although the VPA task has been revised many times e. The requirement is to encode pairs of words e. Testing can be conducted in multiple ways, but one primary outcome measure is performance on a delayed cued recall test i. The VPA task is typically regarded as a verbal memory task.

However, many theories focus on elucidating the role of the hippocampus in visuospatial rather than verbal processing. This includes accounts that consider spatial navigation Maguire et al.

In contrast, the scene construction theory see also the emergent memory account; Graham et al. A scene in this context is a specific type of visual image that represents a naturalistic 3-D space typically populated by objects and that is viewed from an egocentric perspective.

The difficulty with theories such as cognitive map and scene construction is that they do not appear to be able to explain why VPA learning is invariably compromised following hippocampal damage. On the face of it, another hippocampal theory does seem to account for the VPA findings. However, a purely associative account of hippocampal function is not completely satisfactory, given that patients with hippocampal damage retain an ability to form associations in some circumstances.

In taking this issue forward, it is worthwhile first to step back. Examination of the words used in typical VPA tests shows the vast majority are high imagery concrete words. Currently, therefore, standardized VPA tests may be conflating associative processes and imageability. Patients with hippocampal damage are reportedly unable to imagine fictitious and future scenes in addition to their well-reported memory deficits Schacter et al.

It would, therefore, follow that their impoverished scene imagery ability may place them at a disadvantage for processing high imagery concrete words. One way to deal with the conflation of visual imagery and binding is to examine very low imagery abstract word pairs, which would assess binding outside the realm of imagery.

However, abstract word pairs rarely feature in VPA tests used with patients or in neuroimaging experiments. In addition, different types of high imagery words are not distinguished in VPA tests, with the majority of words representing single objects.

It could therefore be that a scene word e. It has also been suggested that even where each word in a pair denotes an object e. Consequently, if visual imagery does play a role in the hippocampal dependence of the VPA task, then it will be important to establish not only whether visual imagery or binding is more relevant but also the type of visual imagery being used.

This allowed us to separate imageability from binding and to examine different types of imagery. Of particular interest were the Object word pairs because we wanted to ascertain whether they were processed using scene or object imagery. For all word pairs, our main interest was during their initial presentation, when any imagery would likely be evoked. In addition, we conducted recognition memory tests after scanning to investigate whether the patterns of hippocampal activity were affected by whether pairs were successfully encoded or not.

Although the VPA memory test used with patients typically involves cued recall, the adaptation of the VPA task for fMRI necessitated the use of recognition memory tests. This is because performing a cued recall test for word pairs that were each seen only once is too difficult even for healthy participants.

We note that recognition memory for word pairs is not often tested in patients, and in the few studies where it has been examined, the results are mixed, with some studies finding a deficit and others a preservation of performance Mayes et al. However, we expected that the use of a recognition memory test instead of cued recall would have limited impact on the patterns of brain activity in this study because we assessed brain activity during the initial presentation of the word pairs and not during memory retrieval.

In line with the scene construction theory, we hypothesized that anterior hippocampal activity would be apparent for Scene words pairs, given the likely evocation of scene imagery. We also predicted that anterior hippocampal activity would be increased for Object word pairs and that this would be best explained by the use of scene imagery. In addition, we expected that the effect of scene imagery use on the hippocampus would be most apparent in high imagery users.

By contrast, we predicted that Abstract words pairs would engage areas outside the hippocampus, even when only subsequently remembered pairs were considered. All were healthy, right-handed, and had normal or corrected-to-normal vision. Given the verbal nature of the task, all participants were highly proficient in English, had English as their first language, and were educated in English throughout their school years. Each participant gave written informed consent.

Therefore, a high score on the VVIQ corresponds to low use of visual imagery. The validity of the VVIQ has been demonstrated in numerous ways. Initially, people completed the VVIQ. Fifteen of the highest and 15 of the lowest scorers made up the low and high imagery groups. A further 15 mid scorers served as the mid imagery group.

We acknowledge that these groups are relatively small for an fMRI study, but we were nevertheless interested to see whether any differences would be observed.

The groups did not differ significantly on age, gender, years of education, and general intellect. Table 1 provides details of the three groups. Table 1. Characteristics of the Participant Groups.

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Verbal Paired Associates and the Hippocampus: The Role of Scenes

Contributor Information. This article has been cited by other articles in PMC. 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.

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