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Purpose: We investigated functional reorganization mechanisms of the human medial temporal lobe (MTL) for episodic memory, in patients suffering from medial temporal lobe epilepsy (MTLE) with hippocampal sclerosis (HS).
Methods: We used functional magnetic resonance imaging (fMRI) to measure brain activity changes during matched episodic encoding tasks of abstract words (Verbal) and line drawings (Visual), in patients with unilateral right MTLE undergoing presurgical evaluation and healthy controls.
Results: As expected, a significant interaction between material type and the side of MTL activity was present in the control group, with preferential involvement of the left hippocampus in verbal encoding and the right parahippocampal region in visual encoding. When compared with controls, right MTLE patients with intact performance activated a region in the left hippocampus more during visual encoding, which resulted in an interaction between group and hemisphere. Importantly, an effect of memory performance on visual encoding activity was observed in the patients, with greater engagement of the left MTL being associated with higher recognition scores. Interestingly, activity in the left MTL also depended on the epileptic seizure frequency, suggesting a role for this clinical parameter in the recruitment of contralateral regions.
Discussion: Taken together, these results indicate functional reorganization of the MTLs in right HS, through transfer of function from the right to the left hemisphere, and strongly suggest an adaptive role for such reorganization mechanism in supporting preserved visual memory.
Since the historical case of patient HM (Scoville & Milner, 1957), it has become a well established finding in memory research that the medial temporal lobes (MTLs) are essential for the encoding, consolidation, and retrieval of episodic memories (Squire et al., 2004). Although still a matter of debate, both regional and hemispheric specializations exist within the MTL. One reasonably consistent finding in both patient and functional imaging studies is the lateralization of MTL activity as a function of material, with the left (dominant) and right (nondominant) MTL structures mediating verbal and visual (nonverbal) memory, respectively (Smith & Milner, 1981; Frisk & Milner, 1990; Kelley et al., 1998; Golby et al., 2001; Powell et al., 2005).
Patients with medial temporal lobe epilepsy (MTLE) often exhibit hippocampal sclerosis (HS), with damage possibly extending to other medial temporal structures but more remote brain regions generally remaining intact (Duncan et al., 1996). Many of these patients have medically refractory seizures and are thus indicated for neurosurgical removal of the epileptogenic area, through anterior temporal lobe resection. Although 60–70% of such cases yield a seizure-free outcome (Wiebe et al., 2001), memory deficits may result, with a differential decline of verbal and nonverbal memory following left and right resection, respectively (Gleissner et al., 2002; Lee et al., 2002). Mapping of MTL memory functions is therefore desirable when planning the surgical resection, in order to minimize postoperative deficits while removing the seizure focus completely (Tharin & Golby, 2007).
Cases of unilateral MTLE provide a unique opportunity to study the long-term consequences of isolated brain damage in episodic memory, because the HS pathology is thought to result from an early-childhood initial precipitating injury inducing functional and structural damage to the hippocampus (Mathern et al., 2002). The fact that patients with early seizure disease onset and severe HS may not show significant changes in memory performance after surgical removal of the epileptogenic MTL suggests that other brain regions can support this function (Jokeit et al., 1999; Gleissner et al., 2002; Dulay et al., 2006). Although functional imaging investigations of individual patients often lack the statistical power to allow conclusive inferences about their MTL function, group studies in unilateral MTLE have already shown that reorganization may occur through transfer of processing to the contralateral MTL (Golby et al., 2002; Richardson et al., 2003; Janszky et al., 2005; Powell et al., 2007a). However, only a few studies have demonstrated an association between memory performance and a pattern of brain activity in MTLE patients that differed from that of normal subjects (Richardson et al., 2003; Powell et al., 2007a) and the significance of these brain activity changes in terms of functional reorganization mechanisms remains to be understood.
The aim of the present study was to investigate the patterns of MTL activity during episodic memory tasks in right MTLE patients and to test the hypothesis that functional reorganization supports preserved visual memory performance in these patients.