Differential contributions of objective memory and mood to subjective memory complaints in refractory focal epilepsy

Abstract

People with epilepsy frequently present with bitter memory complaints. Previous research variously attributes this to symptoms of mood disturbance or objective memory deficits. To investigate the influence of the epileptogenic region on this variability, we examined interrelationships between mood, objective memory, and memory complaints in a sample of patients with refractory focal epilepsy and controls (N = 96). Patients had either mesial temporal (MT, n = 39) or non mesial-temporal (NMT, n = 21) foci. In contrast to controls (n = 36), both patient groups were highly concerned about their memory (P < 0.001) and were more likely to have a history of depression (P = 0.005). Multiple regression showed that objective memory dysfunction and current depressive symptoms predicted the memory complaints of patients with MT epilepsy (P = 0.005), whereas a history of depression predicted the complaints of patients with NMT epilepsy (P = 0.008). These findings suggest that patients have concerns about their memory underpinned by distinct psychological and neurobiological factors depending on the location of their epileptogenic focus.

Introduction

There has been a great deal of research exploring the psychological effects of intractable focal seizures, with mood and memory disturbance emerging as among the most salient comorbid conditions [1], [2]. Stemming from epilepsy research, longstanding importance has been placed on mesial temporal (MT) structures, such as the hippocampus, rhinal cortex, and rhinal–hippocampal interface, for episodic memory [3], [4], [5]. A compromised MT lobe has also been implicated as a marker of vulnerability for depression by diverse structural, genome, and functional neuroimaging studies, including research in epilepsy [1], [6], [7], [8]. Accordingly, patients with MT epilepsy are reported to be more vulnerable to comorbid mood and memory disorders than patients with epileptogenic lesions elsewhere in the brain [1], [3], [9], [10], [11], [12].

Research suggests that there may be a shared neurobiological marker of MT dysfunction underpinning the clinical presentation of mood and memory problems (and their interactions) in MT epilepsy. For instance, impaired objective memory is a common feature of depression [13]. This association has been replicated in the epilepsy population, with the severity of depressive symptoms predicting the extent of objective memory dysfunction in patients with intractable temporal lobe epilepsy (TLE) [14]. Conversely, mood may influence perceived memory deficits in focal epilepsy. O'Shea [15] found that across epilepsy and neurologically healthy samples, affective status accounted for more variance in subjective memory complaint than objective memory performance. Yet despite the well-replicated contribution of depression to subjective memory complaints in epilepsy [16], [17], [18], [19], mood does not always correlate with subjective memory complaints, with other studies attributing the complaints to poor objective memory functioning [20], [21], [22].

In an attempt to elucidate the cause of variability in subjective memory complaints, a few studies have compared groups of patients with differing focal epilepsy syndromes to examine the effect of the epileptogenic location on subjective memory complaints. Overall these findings have been equivocal, with some studies reporting that patients with TLE complain more about their memory than a non-TLE group [21], and others [17] finding no difference in the prevalence of subjective memory concerns between the groups. A recent meta-analysis of the subjective memory literature, however, questioned the validity of previous studies because of their small sample sizes, with non-TLE focal epilepsy groups comprising between 2 and16 participants [23]. Thus, we currently lack systematic investigation of the role of the location of the epileptogenic focus in the subjective memory complaints of people with focal epilepsy.

In summary, despite striking relationships between mood, objective memory, and subjective memory in MT epilepsy, these associations have only been examined in isolation and their interactions remain unknown. In this preliminary study we characterized the mood and memory profiles of patients with refractory focal epilepsy compared with neurologically healthy controls. Because of neurobiological dysfunction in regions crucial for regulating mood and memory, we hypothesized that patients with MT epilepsy would show greater mood disturbance, have poorer objective memory, and therefore complain more about their memory than both patients with NMT epilepsy and controls. This served our main aim of investigating the influence of the epileptogenic region on variability in subjective memory complaints.