Current Literature In Clinical Science

What Happens to the Brain Following Anterior Temporal Lobe Resection?

Memory Network Plasticity After Temporal Lobe Resection: A Longitudinal Functional Imaging Study. Sidhu MK, Stretton J, Winston GP, McEvoy AW, Symms M, Thompson PJ, Koepp MJ, Duncan JS. Brain 2016;139:415–430.

Anterior temporal lobe resection can control seizures in up to 80% of patients with temporal lobe epilepsy. Memory decrements are the main neurocognitive complication. Preoperative functional reorganization has been described in memory networks, but less is known of postoperative reorganization. We investigated reorganization of memoryencoding networks preoperatively and 3 and 12 months after surgery. We studied 36 patients with unilateral medial temporal lobe epilepsy (19 right) before and 3 and 12 months after anterior temporal lobe resection. Fifteen healthy control subjects were studied at three equivalent time points. All subjects had neuropsychological testing at each of the three time points. A functional magnetic resonance imaging memory encoding paradigm of words and faces was performed with subsequent out-of-scanner recognition assessments. Changes in activations across the time points in each patient group were compared to changes in the control group in a single flexible factorial analysis. Postoperative change in memory across the time points was correlated with postoperative activations to investigate the efficiency of reorganized networks. Left temporal lobe epilepsy patients showed increased right anterior hippocampal and frontal activation at both 3 and 12 months after surgery relative to preoperatively, for word and face encoding, with a concomitant reduction in left frontal activation 12 months postoperatively. Right anterior hippocampal activation 12 months postoperatively correlated significantly with improved verbal learning in patients with left temporal lobe epilepsy from preoperatively to 12 months postoperatively. Preoperatively, there was significant left posterior hippocampal activation that was sustained 3 months postoperatively at word encoding, and increased at face encoding. For both word and face encoding this was significantly reduced from 3 to 12 months postoperatively. Patients with right temporal lobe epilepsy showed increased left anterior hippocampal activation on word encoding from 3 to 12 months postoperatively compared to preoperatively. On face encoding, left anterior hippocampal activations were present preoperatively and 12 months postoperatively. Left anterior hippocampal and orbitofrontal cortex activations correlated with improvements in both design and verbal learning 12 months postoperatively. On face encoding, there were significantly increased left posterior hippocampal activations that reduced significantly from 3 to 12 months postoperatively. Postoperative changes occur in the memory-encoding network in both left and right temporal lobe epilepsy patients across both verbal and visual domains. Three months after surgery, compensatory posterior hippocampal reorganization that occurs is transient and inefficient. Engagement of the contralateral hippocampus 12 months after surgery represented efficient reorganization in both patient groups, suggesting that the contralateral hippocampus contributes to memory outcome 12 months after surgery.

Commentary Memory changes are a well-known effect of anterior temporal lobe resection (ATL). Most attention has focused on decreased postoperative memory functioning, with results of a metaanalysis demonstrating memory decline on neuropsychological tests of verbal memory in 44% of individuals undergoing dominant hemisphere ATL, with a rate of decline observed in only 20% of those patients undergoing ATL on the nondominant hemisphere (1). Numerous attempts have been made to Epilepsy Currents, Vol. 16, No. 5 (September/October) 2016 pp. 316–318 © American Epilepsy Society

316

predict which clinical and demographic factors might provide the best predictors for postoperative memory decline. There are also ongoing attempts to modify existing surgical procedures or develop new procedures with the aim of reducing the severity and extent of memory loss associated with most standard surgical approaches (2). Receiving much less attention, however, are those patients who exhibit an improvement in memory functioning following ATL. While general memory improvement has been noted in some studies, Novelly and colleagues were the first to identify this in patients undergoing ATL, a profile selective improvement of modality specific memory functioning associated with the hemisphere contralateral to surgery. In that study’s analysis of group changes, the authors found that patients

What Happens Following Anterior Temporal Lobe Resection?

undergoing left ATL exhibited improvement in recall of visual designs, while those undergoing right ATL demonstrated improvement in paragraph recall (3). Similar findings were seen in other centers. In one investigation that examined individual rates of change using updated versions of the same tests, improvement in delayed recall of visual designs was found in 25% of those patients undergoing left ATL, while improvement in paragraph recall was observed in 31% of right ATL patients (4), indicating that the number of patients obtaining gains in memory performance is apparently comparable to those exhibiting losses. While the field’s emphasis on the investigation and prediction of memory decline in patients undergoing ATL is clearly warranted, the concept of memory gain following surgery is intriguing and may hold a number of important neurobiological and clinical implications for the surgical treatment of epilepsy and prevention of negative postoperative effects. The topic of memory improvement has received relatively little attention to date. Results from neuropsychological investigations have suggested the positive influence of the removal of nociferous brain tissue (5) or the effects of brain plasticity (6). However, while studies using neuropsychological tests have played a prominent role in identifying and measuring the extent of postoperative memory improvement in patients with epilepsy, it is clear that advancing our knowledge of the underlying neurophysiological mechanisms of this improvement requires an addition of advanced neuroimaging techniques. In a recently published investigation, Sidhu and colleagues used functional magnetic resonance imaging (fMRI) to study serial memory changes in 36 patients undergoing ATL (17 left, 19 right) and 15 healthy control subjects. The investigators utilized a memory paradigm involving encoding of words and faces, followed by recognition assessment performed outside of the scanner. Changes in fMRI activation from patients at the time of preoperative testing and at 3 and 12 months following surgery were compared to controls studied at the same intervals. Results from the brain activations during memory encoding were compared to results from the recognition memory testing and to findings from standard neuropsychological tests assessing postoperative memory changes through the use of reliable change indices. This study found two separate dynamic processes underlying memory change in patients undergoing ATL: at 3 months postsurgery, there was evidence of a transient activation of posterior hippocampal regions that was presumed by the authors to be compensatory in nature. This was followed, 12 months after surgery, by an engagement of the hippocampus contralateral to surgery, which was hypothesized to represent the effects of efficient reorganization. Control subjects exhibited rather stable patterns of medial temporal lobe activation on word encoding tests with reduced right-side activations on testing with faces. These data were used to control for longitudinal changes observed in the ATL subjects that were potentially attributed to the effects of repeat testing. Results from this study provide some initial insight on possible neurobiological underpinnings of changes in memory performance following ATL. In their observation of the transitory changes at 3 months, the authors replicated important findings—described in one of their laboratory’s previous

studies performed on an earlier sample—demonstrating that the integrity of the ipsilateral posterior hippocampus is critical to early memory functioning following ATL (7). The demonstration of longer-term changes associated with functioning of contralateral hippocampus now provide a possible explanation of brain changes underlying the memory improvement observed in patients described in previous studies more than 30 years ago (3). It is important to note that findings from this study did not support two of the basic neuropsychological premises that have been described in numerous studies over the years on memory changes following ATL: observing comparable changes at the group level on both the word and face encoding paradigm, the investigators failed to demonstrate any modality specific effects associated with left and right ATL, which is inconsistent with the pattern of findings originally described in early studies on postsurgical memory changes (8). Additionally, the observed pattern of hippocampal activation of the contralateral hemisphere and its prediction of memory outcome at 12 months runs counter to predictions from the functional adequacy model of memory recovery and are more consistent with predictions made by a functional reserve model of postoperative memory functioning (9). The findings from this study may have implications for future research and clinical applications. To begin with, the observed role of the contralateral hippocampus and its relation to memory outcome at 12 months might lead other investigators to reexamine findings from studies using neuropsychological tests, the Wada test, or other fMRI data to determine how contralateral memory functioning, measured preoperatively and in the early stages following surgery, might be used to predict better long-term memory outcome. Additionally, the identification of a possible two-stage process of memory recovery following surgery—engaging different brain regions and possibly different memory encoding strategies—might have important implications for development of novel and dynamic strategies for cognitive remediation at both early and later time points following surgery (10). In the end, one of the most useful lessons gained from the study by Sidhu and colleagues is the demonstration that advanced imaging techniques can be used effectively to address some of the longstanding questions initially raised from neuropsychological studies performed on subjects undergoing ATL. The hope is that, moving into the future, an integrated multidisciplinary approach, using a combination of imaging and neuropsychological methods, can lead to a better understanding of the memory changes observed following ATL and enhance our ability to maximize clinical outcome. by William Barr, PhD References 1. Sherman EM, Wiebe S, Fay-McClymont TB, Tellez-Zenteno J, Metcalfe A, Hernandez-Ronquillo L, Hader WJ, Jetté N. Neuropsychological outcomes after epilepsy surgery: Systematic review and pooled estimates. Epilepsia 2011;52:857–869. 2. Gross RE, Mahmoudi B, Riley JP. Less is more: novel less-invasive surgical techniques for mesial temporal lobe epilepsy that minimize cognitive impairment. Curr Opin Neurol 2015;28:182–191.

317

What Happens Following Anterior Temporal Lobe Resection?

3. Novelly RA, Augustine EA, Mattson RH, Glaser GH, Williamson PD, Spencer DD, Spencer SS. Selective memory improvement and impairment in temporal lobectomy for epilepsy. Ann Neurol 1984;15:64–67. 4. Martin RC, Sawrie SM, Roth DL, Gilliam FG, Faught E, Morawetz RB, Kuzniecky R. Individual memory change after anterior temporal lobectomy: A base rate analysis using regression-based outcome methodology. Epilepsia 1998;39:1075–1082. 5. Hermann B, Seidenberg M. Executive system dysfunction in temporal lobe epilepsy: Effects of nociferous cortex versus hippocampal pathology. J Clin Exp Neuropsychol 1995;17:809–819. 6. Helmstaedter C, Elger CE. Functional plasticity after left anterior temporal lobectomy: Reconstitution and compensation of verbal memory functions. Epilepsia 1998;39:399–406.

318

7. Bonelli SB, Powell RH, Yogarajah M, Samson RS, Symms MR, Thompson PJ, Koepp MJ, Duncan JS. Imaging memory in temporal lobe epilepsy: Predicting the effects of temporal lobe resection. Brain 2010;133(pt 4):1186–1199. 8. Milner B. Psychological aspects of focal epilepsy and its neurosurgical management. Adv Neurol 1975;8:299–321. 9. Chelune GJ. Hippocampal adequacy versus functional reserve: Predicting memory functions following temporal lobectomy. Arch Clin Neuropsychol 1995;10:413–432. 10. Mazur-Mosiewicz A, Carlson HL, Hartwick C, Dykeman J, Lenders T, Brooks BL, Wiebe S. Effectiveness of cognitive rehabilitation following epilepsy surgery: Current state of knowledge. Epilepsia 2015;56:735– 744.

What Happens to the Brain Following Anterior Temporal Lobe Resection?

What Happens to the Brain Following Anterior Temporal Lobe Resection? - PDF Download Free
248KB Sizes 1 Downloads 14 Views