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Background and Objectives
Risk for memory decline is a substantial concern in patients with temporal lobe epilepsy (TLE) undergoing anterior temporal lobectomy (ATL). Although prior studies have identified associations between memory and integrity of white matter (WM) networks within the medial temporal lobe (MTL) pre -operatively, we contribute a...
Contexts in source publication
Context 1
... uncinate fasciculus (UNC) and inferior longitudinal fasciculus (ILF) were selected due to evidence that they are often affected in TLE, 24 contribute to preoperative memory in TLE, [14][15][16]25 and are injured or transected during ATL 26,27 ( Figure 1A). The UNC is a long-range WM tract that connects lateral orbitofrontal cortex and Brodmann area 10 with the anterior temporal lobe. ...
Context 2
... ILF is a long-range associative WM tract that connects the lingual and fusiform areas in the temporo-occipital junction to the anterior temporal cortex. Parahippocampal and entorhinal ROIs were selected based on their strong association with memory, 28 associations with preoperative verbal memory in TLE specifically, 14,29 and with verbal memory decline following ATL 30 ( Figure 1B). ...
Context 3
... also found that integrity of the UNC was an independent predictor of prose memory decline, even after controlling for entorhinal WM integrity and hippocampal volume. The UNC is a long-range WM tract with bidirectional connections between the anterior temporal lobes and frontal cortices ( Figure 1) and is often severed during ATL. 27 Our finding that higher left lateralization of the UNC FA was associated with greater prose memory decline is consistent with preoperative studies linking reduced WM integrity of the UNC to verbal memory impairment. ...
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Citations
... 16 Our group has recently demonstrated that memory outcomes are superior following left ATL when the right-sided UF (reserve) is healthier than the left-sided UF (adequacy) preoperatively. 17 Because the UF is not directly damaged by SLAH, it is not clear if this relationship generalises. Further, the UF represents only the anterior portion of the ventral frontaltemporal network supporting memory function, 18 with the posterior portion consisting of the ILF. ...
... LIs have been used extensively with hippocampal volumes, 35 presurgical fMRI 14 and WM, 36 and were robust predictors of language and memory decline following ATL. 17 LI provides a single measure that takes into account both integrity of the ipsilateral network (structural adequacy) and integrity of the contralateral network (structural reserve). LIs provide powerful estimates because they allow for within-subject normalisation, controlling for variance across individuals and different scan sequences. ...
Background
With expanding neurosurgical options in epilepsy, it is important to characterise each options’ risk for postoperative cognitive decline. Here, we characterise how patients’ preoperative white matter (WM) networks relates to postoperative memory changes following different epilepsy surgeries.
Methods
Eighty-nine patients with temporal lobe epilepsy with T1-weighted and diffusion-weighted imaging as well as preoperative and postoperative verbal memory scores (prose recall) underwent either anterior temporal lobectomy (ATL: n=38) or stereotactic laser amygdalohippocampotomy (SLAH; n=51). We computed laterality indices (ie, asymmetry) for volume of the hippocampus and fractional anisotropy (FA) of two deep WM tracts (uncinate fasciculus (UF) and inferior longitudinal fasciculus (ILF)).
Results
Preoperatively, left-lateralised FA of the ILF was associated with higher prose recall (p<0.01). This pattern was not observed for the UF or hippocampus (ps>0.05). Postoperatively, right-lateralised FA of the UF was associated with less decline following left ATL (p<0.05) but not left SLAH (p>0.05), while right-lateralised hippocampal asymmetry was associated with less decline following both left ATL and SLAH (ps<0.05). After accounting for preoperative memory score, age of onset and hippocampal asymmetry, the association between UF and memory decline in left ATL remained significant (p<0.01).
Conclusions
Asymmetry of the hippocampus is an important predictor of risk for memory decline following both surgeries. However, asymmetry of UF integrity, which is only severed during ATL, is an important predictor of memory decline after ATL only. As surgical procedures and pre-surgical mapping evolve, understanding the role of frontal-temporal WM in memory networks could help to guide more targeted surgical approaches to mitigate cognitive decline.
... The cognitive functions impaired by high sodium intake in the aforementioned animal studies are consistent with functions controlled by the WM tracts, for which we identified correlations between maternal sodium intake and neonatal WM microstructural development. For example, many studies reported memory association with the anterior corona radiate [46,47], parietal white matter [48], posterior limb of internal capsule [49][50][51], external capsule [52,53], and temporal white matter [54]. ...
Maternal diet and nutrient intake are important for fetal growth and development. In this study, we aim to evaluate whether there are associations between maternal diet quality and the offspring’s brain white matter development. Healthy pregnant women’s (N = 44) nutrition intake was assessed by the Healthy Eating Index-2015 (HEI-2015) during the first, second, and third trimesters, respectively. Correlations between MRI diffusion tensor imaging measured fractional anisotropy (FA) of the neonatal brain and the HEI-2015 scores were evaluated using voxel-wise analysis with appropriate multiple comparisons correction and post hoc analysis based on regions of interest. Significant correlations were found between sodium scores at the first trimester of pregnancy and mean neonatal FA values in parietal white matter (R = 0.39, p = 0.01), anterior corona radiata (R = 0.43, p = 0.006), posterior limb of internal capsule (R = 0.53, p < 0.001), external capsule (R = 0.44, p = 0.004), and temporal white matter (R = 0.50, p = 0.001) of the left hemisphere. No other correlations were identified. In conclusion, the relationships between the maternal sodium intake score and the neonatal white matter microstructural development indicate sodium intake patterns better aligned with the Dietary Guidelines for Americans during early pregnancy are associated with greater white matter development in the offspring’s brain.
... Presently, methods of predicting cognitive decline for a given patient rely largely on indices of preoperative functional adequacy of temporal lobe tissue. Patients who perform well on preoperative neuropsychological tests of materialspecific memory (verbal memory in patients with left TLE and visuospatial memory in patients with right TLE), 2,3 who have structurally intact medial temporal lobes, 4,5 and who show greater functional activation in the to-beresected medial temporal lobe during mnemonic processing, as measured with task-based functional magnetic resonance imaging (fMRI), all tend to exhibit the greatest decline in memory after the surgery. [6][7][8] Together, these methods agree, perhaps predictably, that resecting temporal lobe tissue that is functionally healthy is detrimental to memory. ...
... and in-house scripts, individual subject memory network matrices were thresholded and binarized so that only the top positive connections survived at5,10,15,20,25,30,35,40, and 45 percentile connection density thresholds. By calculating several proportional thresholds, in contrast to absolute thresholds, we ensure that all participants' matrices have a similar number of edges, and reduce bias in selecting any one arbitrary threshold. ...
Objective
Predicting memory morbidity after temporal lobectomy in patients with temporal lobe epilepsy (TLE) relies on indices of preoperative temporal lobe structural and functional integrity. However, epilepsy is increasingly considered a network disorder, and memory a network phenomenon. We assessed the utility of functional network measures to predict postoperative memory changes.
Methods
Seventy‐two adults with TLE (37 left/35 right) underwent preoperative resting‐state functional magnetic resonance imaging and pre‐ and postoperative neuropsychological assessment. We compared functional connectivity throughout the memory network of each patient to a healthy control template (n = 19) to identify differences in global organization. A second metric indicated the degree of integration of the to‐be‐resected temporal lobe with the rest of the memory network. We included these measures in a linear regression model alongside standard clinical variables as predictors of memory change after surgery.
Results
Left TLE patients with more atypical memory networks, and with greater functional integration of the to‐be‐resected region with the rest of the memory network preoperatively, experienced the greatest decline in verbal memory after surgery. Together, these two measures explained 44% of variance in verbal memory change, outperforming standard clinical and demographic variables. None of the variables examined was associated with visuospatial memory change in patients with right TLE.
Significance
Resting‐state connectivity provides valuable information concerning both the integrity of to‐be‐resected tissue and functional reserve across memory‐relevant regions outside of the to‐be‐resected tissue. Intrinsic functional connectivity has the potential to be useful for clinical decision‐making regarding memory outcomes in left TLE, and more work is needed to identify the factors responsible for differences seen in right TLE.
... Alternatively, more efficient network organization could be a risk factor for decline due to surgery-driven whole-brain network disruption. 29 Second, as we previously found that left-lateralized MTL white matter integrity at a local level was predictive of memory decline after left anterior temporal lobectomy (ATL), 30 we hypothesized that a greater ipsilateral than contralateral bias of local MTL network organization may lead to greater memory decline after temporal lobe surgery. ...
... We previously found that risk for associative memory decline following left ATL was greater with more leftward asymmetry of MTL white matter integrity, or the health of specific deep white matter tracts and adjoining superficial white matter. 30 We expand upon this to show that beyond integrity, greater leftward MTL network organization produced greater risk for verbal memory decline. A previous fMRI graph theory study reported that better integration of the contralateral hippocampus with the rest of the brain was important for cognitive outcomes, suggestive of functional reserve. ...
Objective:
Risk for memory decline is a common concern for individuals with temporal lobe epilepsy (TLE) undergoing surgery. Global and local network abnormalities are well documented in TLE. However, it is less known whether network abnormalities predict postsurgical memory decline. The authors examined the role of preoperative global and local white matter network organization and risk of postoperative memory decline in TLE.
Methods:
One hundred one individuals with TLE (n = 51 with left TLE and 50 with right TLE) underwent preoperative T1-weighted MRI, diffusion MRI, and neuropsychological memory testing in a prospective longitudinal study. Fifty-six age- and sex-matched controls completed the same protocol. Forty-four patients (22 with left TLE and 22 with right TLE) subsequently underwent temporal lobe surgery and postoperative memory testing. Preoperative structural connectomes were generated via diffusion tractography and analyzed using measures of global and local (i.e., medial temporal lobe [MTL]) network organization. Global metrics measured network integration and specialization. The local metric was calculated as an asymmetry of the mean local efficiency between the ipsilateral and contralateral MTLs (i.e., MTL network asymmetry).
Results:
Higher preoperative global network integration and specialization were associated with higher preoperative verbal memory function in patients with left TLE. Higher preoperative global network integration and specialization, as well as greater leftward MTL network asymmetry, predicted greater postoperative verbal memory decline for patients with left TLE. No significant effects were observed in right TLE. Accounting for preoperative memory score and hippocampal volume asymmetry, MTL network asymmetry uniquely explained 25%-33% of the variance in verbal memory decline for left TLE and outperformed hippocampal volume asymmetry and global network metrics. MTL network asymmetry alone produced good diagnostic classification of memory decline in left TLE (i.e., an area under the receiver operating characteristic curve of 0.80-0.84 and correct classification of 65%-76% of cases with cross-validation).
Conclusions:
These preliminary data suggest that global white matter network disruption contributes to verbal memory impairment preoperatively and predicts postsurgical verbal memory outcomes in left TLE. However, a leftward asymmetry of MTL white matter network organization may confer the highest risk for verbal memory decline. Although this requires replication in a larger sample, the authors demonstrate the importance of characterizing preoperative local white matter network properties within the to-be-operated hemisphere and the reserve capacity of the contralateral MTL network, which may eventually be useful in presurgical planning.
... Presently, methods of predicting cognitive decline for a given patient rely largely on indices of preoperative functional adequacy of temporal lobe tissue. Patients who perform well on preoperative neuropsychological tests of material-specific memory (verbal memory in patients with left TLE and visuospatial memory in patients with right TLE) 2,3 , who have structurally intact medial temporal lobes 4,5 , and who show greater functional activation in the to-be-resected medial temporal lobe during mnemonic processing, as measured with task-based fMRI, all tend to exhibit the greatest decline in memory after the surgery [6][7][8] . Together these methods agree, perhaps predictably, that resecting temporal lobe tissue that is functionally healthy is detrimental to memory. ...
... Using the Brain Connectivity Toolbox (https://sites.google.com/site/bctnet/) 34 and in-house scripts, individual subject memory network matrices were thresholded and binarized so that only the top positive connections survived at 5,10,15,20,25,30,35,40, and 45 percentile connection density thresholds. By calculating several proportional thresholds, in contrast to absolute thresholds, we ensure that all participants' matrices have similar number of edges, and reduce bias in selecting any one arbitrary threshold 34 . ...
Objectives
Anterior temporal lobectomy as a treatment for temporal lobe epilepsy is associated with a variable degree of postoperative memory decline, and estimating this decline for individual patients is a critical step of preoperative planning. Presently, predicting memory morbidity relies on indices of preoperative temporal lobe structural and functional integrity. However, epilepsy is increasingly understood as a network disorder, and memory a network phenomenon. We aimed to assess the utility of functional network measures to predict postoperative memory changes.
Methods
Patients with left and right temporal lobe epilepsy (TLE) were recruited from an epilepsy clinic. Patients underwent preoperative resting-state fMRI (rs-fMRI) and pre- and postoperative neuropsychological assessment approximately one year after surgery. We compared functional connectivity throughout the memory network of each patient to a healthy control template based on 19 individuals to identify differences in global organization. A second metric indicated the degree of integration of the to-be-resected temporal lobe with the rest of the memory network. We included these measures in a linear regression model alongside standard clinical and demographic variables as predictors of memory change after surgery.
Results
Seventy-two adults with TLE were included in this study (37 left/35 right). Left TLE patients with more abnormal memory networks, and with greater functional integration of the to-be-resected region with the rest of the memory network preoperatively, experienced the greatest decline in verbal memory after surgery. Together, these two measures explained 44% of variance in verbal memory change (F(2,31)=12.01, p=0.0001), outperforming standard clinical and demographic variables. None of the variables examined in this study were associated with visuospatial memory change in patients with right TLE.
Conclusion
Resting-state connectivity provides valuable information concerning both the integrity of to-be-resected tissue as well as functional reserve across memory-relevant regions outside of the to-be-resected tissue. Intrinsic functional connectivity has the potential to be useful for clinical decision-making regarding memory outcomes in left TLE, and more work is needed to identify the factors responsible for differences seen in right TLE.
Epilepsy is a common neurological disorder associated with alterations in cortical and subcortical brain networks. Despite a historical focus on gray matter regions involved in seizure generation and propagation, the role of white matter (WM) network disruption in epilepsy and its comorbidities has sparked recent attention. In this review, we describe patterns of WM alterations observed in focal and generalized epilepsy syndromes and highlight studies linking WM disruption to cognitive and psychiatric comorbidities, drug resistance, and poor surgical outcomes. Both tract-based and connectome-based approaches implicate the importance of extratemporal and temporo-limbic WM disconnection across a range of comorbidities, and an evolving literature reveals the utility of WM patterns for predicting outcomes following epilepsy surgery. We encourage new research employing advanced analytic techniques (e.g., machine learning) that will further shape our understanding of epilepsy as a network disorder and guide individualized treatment decisions. We also address the need for research that examines how neuromodulation and other treatments (e.g., laser ablation) affect WM networks, as well as research that leverages larger and more diverse samples, longitudinal designs, and improved magnetic resonance imaging acquisitions. These steps will be critical to ensuring generalizability of current research and determining the extent to which neuroplasticity within WM networks can influence patient outcomes.
