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.

Keywords: anterior temporal lobe resection; functional MRI; temporal lobe epilepsy; verbal memory; visual memory.

Figure 1

Postoperative group results in patients with left TLE. Postoperative main effects for: word encoding, left posterior hippocampal activation; face encoding, left and right hippocampal activation. Yellow line indicates the estimated hippocampal resection margin for the left TLE group (threshold P < 0.01, uncorrected). Significant regions are superimposed onto averaged normalized mean echo planar images from all patients who underwent left ATLR.

Figure 2

Comparison of post- and preoperative functional MRI activation for verbal memory function in left TLE. Main effects: greater postoperative than preoperative activation for encoding words in the left posterior medial temporal lobe four months after left ATLR. Yellow line indicates the estimated hippocampal resection margin for the left TLE group. Threshold P < 0.01, uncorrected. Significant regions are superimposed onto an averaged normalized mean echo planar image from all patients who underwent left ATLR.

Figure 3

Efficiency of preoperative reorganization of verbal memory function in left TLE. Correlational analysis: greater pre- than postoperative activation on encoding words in the left posterior medial temporal lobe is associated with better verbal learning outcome. Yellow line indicates the estimated hippocampal resection margin for the left TLE group (threshold P < 0.01, uncorrected). Significant regions are superimposed onto averaged normalized mean echo planar images from all patients who underwent left ATLR.

Figure 4

Efficiency of postoperative reorganization of verbal memory function in left TLE. Correlational analysis: Greater post- than preoperative left posterior medial temporal lobe functional MRI activation for word encoding correlates with worse postoperative verbal learning scores, characterized by an inefficient postoperative response within the remaining ipsilateral posterior medial temporal lobe structures. The correlation at the peak voxel in the left posterior medial temporal lobe (MTL) is illustrated. ‘Functional MRI activation’ is given in ‘postoperative > preoperative percent signal change’; scores for ‘verbal learning’ are given as z-scores. Yellow line indicates the estimated hippocampal resection margin for the left TLE group. Threshold P < 0.01, uncorrected. Significant regions are superimposed onto an averaged normalized mean echo planar images from all patients who underwent left ATLR.