Accelerated long-term forgetting in transient epileptic amnesia: An acquisition or consolidation deficit?

Abstract

Accelerated Long-term Forgetting (ALF) is the rapid loss of newly acquired memories over days to weeks despite normal retention at standard (~30min) intervals. It has recently been described in association with epilepsy, particularly the syndrome of Transient Epileptic Amnesia (TEA). The cognitive mechanisms underlying ALF remain uncertain, but disruption either of memory acquisition or consolidation processes has been postulated. To arbitrate between these accounts, we reanalysed data from an existing word-list recall data set to investigate whether ALF can be observed for words learned under precisely matched conditions in TEA patients and controls. We reanalysed the data of 24 patients with TEA and 24 matched healthy controls who learnt a 15-item word list to a learning criterion of 90% with a minimum of five learning trials. Free recall of the words was probed at delays of 30min and 1 week and 3 weeks after learning. In addition, a ‘yes–no’ recognition test was conducted after the 3-week free recall. Forgetting rates across the first 30min delay and the subsequent 1 week and 3 week delay were compared between patients and controls. To ensure that learning conditions were closely matched between patients and control participants, we excluded exceptionally fast (NTEA=1, Ncontrols=4) and slow (NTEA=6, Ncontrols=2) learners. Furthermore, we analysed only words that were presented five or six times during learning and retrieved successfully on four or five occasions during learning. Recall performance on the last learning trial and 30min after acquisition were indistinguishable between TEA patients and controls. Over the delay interval of 30min to 1 week, however, accelerated forgetting of this newly learned verbal material was observed in TEA patients. This severe forgetting is also reflected in the three-week recognition test, where TEA patients performed significantly worse than controls. Moreover, whereas recall on the last learning trial correlated significantly with the 30min delayed recall in both groups, recall on the last learning trial correlated significantly with 1 week and 3 week delayed recall only in the controls. In both groups, the three-week free recall performance correlated with the three-week recognition test. Patients with TEA demonstrate ALF even for verbal material that is learned under precisely matched conditions. These results are consistent with the hypothesis that ALF represents a disruption of memory consolidation rather than an acquisition deficit.