Examining factors related to accelerated long‐term forgetting in epilepsy using ambulatory EEG monitoring

Abstract

Summary Purpose Some patients with epilepsy demonstrate normal memory when this is tested at relatively short intervals (e.g., 30 min), but substantial loss over longer delay periods (e.g., days or weeks) when compared to healthy control subjects. This pattern of “accelerated long‐term forgetting” (ALF) affects the everyday lives of patients, yet goes undetected by standard neuropsychological memory tests, and its pathophysiologic basis is poorly understood. By testing memory over a period of concurrent ambulatory electroencephalography (EEG), the current study aimed to investigate possible factors contributing to ALF. Methods Thirty‐nine patients diagnosed with epilepsy or probable epilepsy underwent 5 days of continuous ambulatory EEG: 18 had normal EEG studies, 10 had focal epileptic discharges, 5 had generalized epileptic discharges, and 6 had one or more seizures. Fifteen matched healthy control subjects also participated, but did not undergo EEG. Subjects were taught 13‐item word and design lists to criterion, and recall was tested at 30 min, 24 h, and 4 days. Subjects also completed questionnaires pertaining to everyday memory and mood. Key Findings Group analyses (excluding patients who experienced seizures during monitoring) indicated that patients who experienced generalized discharges during the 24‐h to 4‐day delay intervals showed higher rates of forgetting for nonverbal information. Those with focal discharges showed ALF between 30 min and 4 days for verbal information, whereas those with normal EEGs over the 4 days recording had no evidence of ALF. Surprisingly, mood and epilepsy variables (such as duration of disease or number of anticonvulsant medications) showed no significant correlation with ALF. Although no aspect of nighttime sleep architecture was found to be related to recall after the first 24 h, daytime naps were associated with better retention. Self‐report of everyday memory functioning was related to recall at longer delays, but not at 30 min. Significance The present findings indicated that ALF in epilepsy is associated with subclinical discharges rather than antiepileptic drugs (AEDs), mood or sleep disturbance. Measures of longer‐term recall can reveal correlations with subjective everyday memory complaints that are not evident when recall is only tested at a standard (30 min) delay interval. These findings have the potential to improve treatment strategies for patients who complain of memory difficulties.

The impact of epileptiform abnormalities and hippocampal lesions on retention of recent autobiographical experiences: Adding insult to injury?

“…In support of this, both Mameniskiene et al (2006) and Fitzgerald et al (2013) found that the presence of epileptiform discharges was associated with ALF for word lists and designs. Whether this might be true for other types of material has not yet been tested (e.g., autobiographical events).…”

“…Mameniskiene et al (2006) found that both seizures and interictal discharges affected verbal and nonverbal recall at four weeks delay. Similarly, Fitzgerald et al (2013) found that discharges affected retention of word and design lists at four days delay. The present results add evidence that epileptiform activity also disrupts consolidation of incidentally encoded event information and that this effect becomes more obvious over longer timeframes.…”

“…Also, there have been some reports of improved anterograde memory with the commencement of AEDs in both TEA and TLE patients (Midorikawa and Kawamura, 2007;O'Connor et al, 1997;Zeman et al, 1998). Lah et al (2006) also found a negative association between number of AEDs and amount recalled on a test of remote autobiographical memory, But when Fitzgerald et al (2013) considered the number of AEDs patients were taking, they found no relationship between this variable and word or design list retention over a four day period. Further investigation of this potentially relevant factor is important from a clinical perspective.…”

“…Some patients with epilepsy show accelerated long-term forgetting (ALF) over days or weeks for material demonstrated to have been retained when assessed after short-term delays (e.g., Fitzgerald et al, 2013;Kapur et al, 1997;Narayanan et al, 2012;Tramoni et al, 2011). There are also epilepsy patients who show a pattern of ALF in addition to impaired performance at short delays (Mameniskiene et al, 2006;Wilkinson et al, 2011).…”

“…Many studies (Cheung et al, 2006;Cipolotti and Bird, 2006;Milner, 1975;Sass et al, 1990;Spiers, Maguire et al, 2001) have examined factors that influence memory at shorter delay intervals (e.g., 30-60 min), and recently there have been efforts to discover if the same factors also influence longer term memory formation. In addition, some researchers have considered whether the occurrence of seizures/interictal epileptiform discharges during the delay contribute to memory impairments over longer intervals (e.g., Fitzgerald et al, 2013;Mameniskiene et al, 2006;Wilkinson et al, 2011). What is known about these factors will be reviewed here.…”