Association Between Microstructural Asymmetry of Temporal Lobe White Matter and Memory Decline After Anterior Temporal Lobectomy

Stasenko, Alena; Kaestner, Erik; Reyes, Anny; Lalani, Sanam J.; Paul, Brianna M.; Hegde, Manu; Ben-Haim, Sharona; McDonald, Carrie R.

doi:10.1212/wnl.0000000000200047

Cited by 8 publications

(8 citation statements)

References 55 publications

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“…Consideration of the asymmetry of the MTL network is important because it takes into account both integrity of the ipsilateral network ( structural adequacy) as well as integrity or presumed “functionality” of the contralateral network ( structural reserve) to predict memory outcomes. We previously found that risk for associative memory decline in L-TLE was greater with more leftward (i.e., ipsilateral) asymmetry of MTL white matter integrity (i.e., health of specific tracts and adjoining superficial white matter 29 . We expand upon this and show that beyond integrity, greater ipsilateral (than contralateral) MTL network organization produced a greater risk for list-learning decline.…”

Section: Discussionmentioning

confidence: 97%

“…Alternatively, more efficient network organization could be a risk factor for greater decline due to the risk of surgery-driven whole brain network disruption 28 . Second, given that we previously found that left-lateralized MTL white matter integrity at a local level was predictive of memory decline in L-TLE 29 , we hypothesized that greater ipsilateral than contralateral bias of local MTL network organization may lead to greater memory decline after temporal lobe surgery.…”

Section: Introductionmentioning

confidence: 99%

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White matter network organization predicts memory decline after epilepsy surgery

Stasenko

Kaestner

Arienzo

et al. 2023

Preprint

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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 post-surgical memory decline. We examined the role of pre-operative global and local white matter network organization in risk for post-operative memory decline in TLE. One-hundred one individuals with TLE (51 left; L-TLE) and 56 controls underwent T1-weighted, diffusion-MRI and neuropsychological memory testing in a prospective longitudinal study. Forty-four patients subsequently underwent temporal lobe surgery and post-operative memory testing. Structural connectomes were generated via tractography and analyzed using measures of global (integration and specialization) and local (medial temporal lobe [MTL] specialization) network organization. Pre-operatively, higher global network integration and specialization were associated with higher verbal memory function in L-TLE. Higher pre-operative global network integration and specialization, as well as more leftward local specialization, predicted greater post-surgical verbal memory decline for L-TLE. Accounting for pre-operative memory score and hippocampal volume asymmetry, local network specialization additionally explained 25-33% of the variance in outcomes for L-TLE and outperformed hippocampal asymmetry. Local network specialization alone produced good diagnostic accuracy (AUC=.80-.84) in L-TLE. Global white matter network disruption contributes to verbal memory impairment pre-operatively and predicts post-surgical memory outcomes in L-TLE. However, leftward asymmetry of MTL network organization confers the highest risk for memory decline. This demonstrates the importance of characterizing local network properties within the to-be-operated hemisphere and the reserve capacity of the contralateral MTL network.

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Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

White matter network organization predicts memory decline after epilepsy surgery

Stasenko

Kaestner

Arienzo

et al. 2023

Preprint

Self Cite

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“…We found no significant differences in age between the three groups ( 2 (2)=2.85, p=0.24; left TLE/right TLE/control), nor were there differences in sex ( 2 (2)=2.57, p=0.28). However, there were differences in education (F(2,86)=12.83, p=0.000013) due to higher levels of education in controls than both patient groups (control vs left TLE: W=524.5, p=0.000082, MedianDiff=3, CI [2][3][4][5]; control vs right TLE: t(50)=4.33, p=0.000073, CI [1.95-5.33]). Years of education between the left and right TLE groups was not reliably different W=669.5, p=0.81, MedianDiff=0.00002, CI[-1-1]), nor was age of onset (W=558, p=0.32, MedianDiff=-3, CI[-11-3]).…”

Section: Participant Demographicsmentioning

confidence: 99%

“…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.…”

Section: Introductionmentioning

confidence: 99%

Leveraging the resting brain to predict memory decline after temporal lobectomy

Audrain

Barnett

McAndrews

2022

Preprint

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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.

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“…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.…”

Section: Introductionmentioning

confidence: 99%

Leveraging the resting brain to predict memory decline after temporal lobectomy

Audrain,

Barnett,

Mouseli

et al. 2023

Epilepsia

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ObjectivePredicting 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.MethodsSeventy‐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.ResultsLeft 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.SignificanceResting‐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.

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Association Between Microstructural Asymmetry of Temporal Lobe White Matter and Memory Decline After Anterior Temporal Lobectomy

Cited by 8 publications

References 55 publications

White matter network organization predicts memory decline after epilepsy surgery

White matter network organization predicts memory decline after epilepsy surgery

Leveraging the resting brain to predict memory decline after temporal lobectomy

Leveraging the resting brain to predict memory decline after temporal lobectomy

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