Memory reorganization following anterior temporal lobe resection: a longitudinal functional MRI study

Abstract

Anterior temporal lobe resection controls seizures in 50–60% of patients with intractable temporal lobe epilepsy but may impair memory function, typically verbal memory following left, and visual memory following right anterior temporal lobe resection. Functional reorganization can occur within the ipsilateral and contralateral hemispheres. We investigated the reorganization of memory function in patients with temporal lobe epilepsy before and after left or right anterior temporal lobe resection and the efficiency of postoperative memory networks. We studied 46 patients with unilateral medial temporal lobe epilepsy (25/26 left hippocampal sclerosis, 16/20 right hippocampal sclerosis) before and after anterior temporal lobe resection on a 3 T General Electric magnetic resonance imaging scanner. All subjects had neuropsychological testing and performed a functional magnetic resonance imaging memory encoding paradigm for words, pictures and faces, testing verbal and visual memory in a single scanning session, preoperatively and again 4 months after surgery. Event-related analysis revealed that patients with left temporal lobe epilepsy had greater activation in the left posterior medial temporal lobe when successfully encoding words postoperatively than preoperatively. Greater pre- than postoperative activation in the ipsilateral posterior medial temporal lobe for encoding words correlated with better verbal memory outcome after left anterior temporal lobe resection. In contrast, greater postoperative than preoperative activation in the ipsilateral posterior medial temporal lobe correlated with worse postoperative verbal memory performance. These postoperative effects were not observed for visual memory function after right anterior temporal lobe resection. Our findings provide evidence for effective preoperative reorganization of verbal memory function to the ipsilateral posterior medial temporal lobe due to the underlying disease, suggesting that it is the capacity of the posterior remnant of the ipsilateral hippocampus rather than the functional reserve of the contralateral hippocampus that is important for maintaining verbal memory function after anterior temporal lobe resection. Early postoperative reorganization to ipsilateral posterior or contralateral medial temporal lobe structures does not underpin better performance. Additionally our results suggest that visual memory function in right temporal lobe epilepsy is affected differently by right anterior temporal lobe resection than verbal memory in left temporal lobe epilepsy.

Risk Reduction in Dominant Temporal Lobe Epilepsy Surgery Combining fMRI/DTI Maps, Neuronavigation and Intraoperative 1.5-Tesla MRI

“…There is an ongoing debate about the ability of postoperative compensation for verbal memory decline after surgery of the posterior parts of the ipsilateral hippocampus versus contralateral temporomesial structures [37]. We found a relevant fMRI memory-related cortical area within the posterior parahippocampal gyrus, which influenced the postoperative memory outcome more positively when preserved than small hippocampal resection (fig.…”

Applications of Blood-Oxygen-Level-Dependent Functional Magnetic Resonance Imaging and Diffusion Tensor Imaging in Epilepsy

“…2). 78 Others have suggested that postoperative visual and verbal memory performance is positively associated with the activation of contralateral medial temporal lobe and its connectivity to posterior cingulate cortex ipsilateral to the sclerosed hippocampus after temporal lobe resection. 85 …”

Memory Assessment in the Clinical Context Using Functional Magnetic Resonance Imaging

“…In addition, one study reported that increased activation in the posterior MTL following anterior temporal lobe resection in patients with left mTLE was actually correlated with worse postoperative verbal memory performance. 51 The question of whether "more is better" in terms of activation magnitude is discussed again later.…”

“…Using the probability of clinically meaningful postoperative decline in mTLE as an example, would 3 activated voxels present no risk whereas 15 would signify a strong risk? Although few studies have attempted to quantify this, Bonelli and colleagues 51 reported that activation of the MTL alone showed poor PPV (20%-30%, depending on hemisphere), but also that it did significantly contribute to strong prediction when language lateralization and preoperative test performance were included in the models (PPV 70% for left mTLE/verbal memory change and 100% for right mTLE and visual memory change). Overall, the field is not sufficiently mature to have highly reliable activation tasks or rsFC metrics with appropriate cutoffs for clinical decision making, but this issue is likely years rather than decades away from being resolved.…”