Abstract
Progressive gray matter volume reductions beyond the epileptogenic area has been described in temporal lobe epilepsy. There is less evidence regarding correlations between gray and white matter volume changepres and multi-domain cognitive performance in this setting. We aimed to investigate correlations between volume changes in parietal structures and visuospatial performance in temporal lobe epilepsy patients. we performed a cross-sectional study comparing global and regional brain volume data from 34 temporal lobe epilepsy patients and 30 healthy controls. 3D T1-weighted sequences were obtained on a 3.0 T magnet, and data were analyzed using age and sex-adjusted linear regression models. Global and regional brain volumes and cortical thickness in patients were correlated with standardized visual memory, visuoperceptual, visuospatial, and visuoconstructive parameters obtained in a per-protocol neuropsychological assessment. temporal lobe epilepsy patients had smaller volume fractions of the deep gray matter structures, putamen and nucleus accumbens, and larger cerebrospinal fluid volume fraction than controls. Correlations were found between: 1) visual memory and precuneus and inferior parietal cortical thickness; 2) visuoperceptual performance and precuneus and supramarginal white matter volumes; 3) visuospatial skills and precuneus, postcentral, and inferior and superior parietal white matter volumes; 4) visuoconstructive performance and inferior parietal white matter volume. Brain volume loss is widespread in temporal lobe epilepsy. Volumetric reductions in parietal lobe structures were associated with visuoperceptual cognitive performance.
Similar content being viewed by others
Data availability
Anonymized data that support the findings of this study are available from the authors on reasonable request.
Code availability
Not applicable.
References
AJ, S., MF, H., & SD, D. (1997). Some Comments on Frequently Used Multiple Endpoint Adjustment Methods in Clinical Trials. Statistics in medicine, 16(22). https://doi.org/10.1002/(SICI)1097-0258(19971130)16:22<2529::AID-SIM692>3.0.CO;2-J
Allone, C., Lo Buono, V., Corallo, F., Pisani, L. R., Pollicino, P., Bramanti, P., & Marino, S. (2017). Neuroimaging and cognitive functions in temporal lobe epilepsy: A review of the literature. Journal of the neurological sciences, 381, 7–15. https://doi.org/10.1016/j.jns.2017.08.007
Barr, W. B., Chelune, G. J., Hermann, B. P., Loring, D. W., Perrine, K., Strauss, E., et al. (1997). The use of figural reproduction tests as measures of nonverbal memory in epilepsy surgery candidates. Journal of the International Neuropsychological Society, 3(5), 435–443. https://doi.org/10.1017/S1355617797004359
Bentvelzen, A. C., Kessels, R. P. C., Badcock, N. A., & Savage, G. (2021). The Impact of Right Temporal Lobe Epilepsy On Nonverbal Memory: Meta-regression of Stimulus- and Task-related Moderators. Neuropsychology Review, 2021, 1–21. https://doi.org/10.1007/S11065-021-09514-3
Bernhardt, B. C., Worsley, K. J., Kim, H., Evans, A. C., Bernasconi, A., & Bernasconi, N. (2009). Longitudinal and cross-sectional analysis of atrophy in pharmacoresistant temporal lobe epilepsy. Neurology, 72(20), 1747–1754. https://doi.org/10.1212/01.wnl.0000345969.57574.f5
Bernhardt, B. C., Bernasconi, N., Concha, L., & Bernasconi, A. (2010). Cortical thickness analysis in temporal lobe epilepsy: reproducibility and relation to outcome. Neurology, 74(22), 1776–1784. https://doi.org/10.1212/WNL.0b013e3181e0f80a
Blümcke, I., Thom, M., Aronica, E., Armstrong, D. D., Bartolomei, F., Bernasconi, A., et al. (2013). International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: A Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia, 54(7), 1315–1329. https://doi.org/10.1111/epi.12220
Bonilha, L., Kobayashi, E., Rorden, C., Cendes, F., & Li, L. M. (2003). Medial temporal lobe atrophy in patients with refractory temporal lobe epilepsy. Journal of neurology, neurosurgery, and psychiatry, 74(12), 1627–1630. https://doi.org/10.1136/jnnp.74.12.1627
Bonilha, L., & Keller, S. S. (2015). Quantitative MRI in refractory temporal lobe epilepsy: relationship with surgical outcomes. Quantitative imaging in medicine and surgery, 5(2), 204–224. https://doi.org/10.3978/j.issn.2223-4292.2015.01.01
Caciagli, L., Bernasconi, A., Wiebe, S., Koepp, M. J., Bernasconi, N., & Bernhardt, B. C. (2017). A meta-analysis on progressive atrophy in intractable temporal lobe epilepsy: Time is brain? Neurology, 89(5), 506–516. https://doi.org/10.1212/WNL.0000000000004176
Chang, Y. A., Marshall, A., Bahrami, N., Mathur, K., Javadi, S. S., Reyes, A., et al. (2019). Differential sensitivity of structural, diffusion, and resting-state functional <scp>MRI</scp> for detecting brain alterations and verbal memory impairment in temporal lobe epilepsy. Epilepsia, 60(5), 935–947. https://doi.org/10.1111/epi.14736
Coan, A. C., Appenzeller, S., Bonilha, L., Li, L. M., & Cendes, F. (2009). Seizure frequency and lateralization affect progression of atrophy in temporal lobe epilepsy. Neurology, 73(11), 834–842. https://doi.org/10.1212/WNL.0b013e3181b783dd
Currie, S., Heathfield, K. W. G., Henson, R. A., & Scott, D. F. (1971). Clinical course and prognosis of temporal lobe epilepsy: A survey of 666 patients. Brain, 94(1), 173–190. https://doi.org/10.1093/brain/94.1.173
De Schotten, M. T., Dell’Acqua, F., Forkel, S. J., Simmons, A., Vergani, F., Murphy, D. G. M., & Catani, M. (2011). A lateralized brain network for visuospatial attention. Nature Neuroscience, 14(10), 1245–1246. https://doi.org/10.1038/nn.2905
Fischl, B., & Dale, A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America, 97(20), 11050. https://doi.org/10.1073/PNAS.200033797
FreeSurferAnalysisPipelineOverview - Free Surfer Wiki. (n.d.). http://surfer.nmr.mgh.harvard.edu/fswiki/FreeSurferAnalysisPipelineOverview. Accessed 4 March 2020.
Fu, J., Liu, Y., Yang, K., Long, H., Wang, K., & Qi, S. (2018). Effect of accumbens nucleus shell lesioning on bitemporal lobe epilepsy in rat model. Folia Neuropathologica, 56(4), 346–353. https://doi.org/10.5114/fn.2018.80868
Galovic, M., van Dooren, V. Q. H., Postma, T., Vos, S. B., Caciagli, L., Borzì, G., et al. (2019). Progressive Cortical Thinning in Patients With Focal Epilepsy. JAMA Neurology. https://doi.org/10.1001/jamaneurol.2019.1708
Grant, A. C., Henry, T. R., Fernandez, R., Hill, M. A., & Sathian, K. (2005). Somatosensory processing is impaired in temporal lobe epilepsy. Epilepsia, 46(4), 534–539. https://doi.org/10.1111/j.0013-9580.2005.54604.x
Grant, A. C., Donnelly, K. M., Chubb, C., Barr, W. B., Kuzniecky, R., & Devinsky, O. (2008). Temporal lobe epilepsy does not impair visual perception. Epilepsia, 49(4), 710–713. https://doi.org/10.1111/j.1528-1167.2007.01483.x
Hedderich, D. M., Drost, R., Goldhardt, O., Ortner, M., Müller-Sarnowski, F., Diehl-Schmid, J., et al. (2020). Regional Cerebral Associations Between Psychometric Tests and Imaging Biomarkers in Alzheimer’s Disease. Article, 11, 1. https://doi.org/10.3389/fpsyt.2020.00793
Helmstaedter, C., & Kockelmann, E. (2006). Cognitive outcomes in patients with chronic temporal lobe epilepsy. Epilepsia, 47(SUPPL. 2), 96–98. https://doi.org/10.1111/j.1528-1167.2006.00702.x
Hermann, B. P., Seidenberg, M., Dow, C., Jones, J., Rutecki, P., Bhattacharya, A., & Bell, B. (2006). Cognitive prognosis in chronic temporal lobe epilepsy. Annals of Neurology, 60(1), 80–87. https://doi.org/10.1002/ana.20872
Jber, M., Habibabadi, J. M., Sharifpour, R., Marzbani, H., Hassanpour, M., Seyfi, M., et al. (2021). Temporal and extratemporal atrophic manifestation of temporal lobe epilepsy using voxel-based morphometry and corticometry: clinical application in lateralization of epileptogenic zone. Neurological sciences: official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology, 42(8), 3305–3325. https://doi.org/10.1007/S10072-020-05003-2
Kalilani, L., Sun, X., Pelgrims, B., Noack-Rink, M., & Villanueva, V. (2018). The epidemiology of drug-resistant epilepsy: A systematic review and meta-analysis. Epilepsia, 59(12), 2179–2193. https://doi.org/10.1111/EPI.14596
Keller, S. S., & Roberts, N. (2008). Voxel-based morphometry of temporal lobe epilepsy: An introduction and review of the literature. Epilepsia, 49(5), 741–757. https://doi.org/10.1111/j.1528-1167.2007.01485.x
Kim, J. S., Koo, D. L., Joo, E. Y., Kim, S. T., Seo, D. W., & Hong, S. B. (2016). Asymmetric Gray Matter Volume Changes Associated with Epilepsy Duration and Seizure Frequency in Temporal-Lobe-Epilepsy Patients with Favorable Surgical Outcome. Journal of Clinical Neurology, 12(3), 323. https://doi.org/10.3988/jcn.2016.12.3.323
Kwan, P., Arzimanoglou, A., Berg, A. T., Brodie, M. J., Allen Hauser, W., Mathern, G., et al. (2010). Definition of drug resistant epilepsy: consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies. Epilepsia, 51(6), 1069–1077. https://doi.org/10.1111/j.1528-1167.2009.02397.x
Leech, R., & Sharp, D. J. (2014). The role of the posterior cingulate cortex in cognition and disease. Brain. Oxford University Press. https://doi.org/10.1093/brain/awt162
Liu, Z., Xu, Y., An, J., Wang, J., Yin, X., Huang, R., et al. (2015). Altered Brain White Matter Integrity in Temporal Lobe Epilepsy: A TBSS Study. Journal of Neuroimaging, 25(3), 460–464. https://doi.org/10.1111/jon.12154
Lopez, S. M., Aksman, L. M., Oxtoby, N. P., Vos, S. B., Rao, J., Kaestner, E., et al. (2022). Event-based modelling in temporal lobe epilepsy demonstrates progressive atrophy from cross-sectional data. Epilepsia. https://doi.org/10.1111/EPI.17316
McDonald, C. R., Busch, R. M., Reyes, A., Arrotta, K., Barr, W., Block, C., et al. (2022). Development and application of the International Classification of Cognitive Disorders in Epilepsy (IC-CoDE): Initial results from a multi-center study of adults with temporal lobe epilepsy. Neuropsychology. https://doi.org/10.1037/NEU0000792
Neal, E. G., Di, L., Reale-Caldwell, A. R., Maciver, S., Schoenberg, M. R., & Vale, F. L. (2019). Network connectivity separate from the hypothesized irritative zone correlates with impaired cognition and higher rates of seizure recurrence. Epilepsy and Behavior, 101. https://doi.org/10.1016/j.yebeh.2019.106585
Riederer, F., Seiger, R., Lanzenberger, R., Pataraia, E., Kasprian, G., Michels, L., et al. (2020). Voxel-based morphometry-from hype to hope. A study on hippocampal atrophy in mesial temporal lobe epilepsy. American Journal of Neuroradiology, 41(6), 987–993. https://doi.org/10.3174/ajnr.A6545
Scheffer, I. E., Berkovic, S., Capovilla, G., Connolly, M. B., French, J., Guilhoto, L., et al. (2017). ILAE classification of the epilepsies: Position paper of the ILAE Commission for Classification and Terminology. Epilepsia, 58(4), 512–521. https://doi.org/10.1111/epi.13709
Seydell-Greenwald, A., Ferrara, K., Chambers, C. E., Newport, E. L., & Landau, B. (2017). Bilateral parietal activations for complex visual-spatial functions: Evidence from a visual-spatial construction task. Neuropsychologia, 106, 194–206. https://doi.org/10.1016/j.neuropsychologia.2017.10.005
Sheldon, S., Heydari, N., Cole, J., & Hamberger, M. J. (2020). Intraindividual relative deficits in visual memory to lateralize seizure onset in temporal lobe epilepsy. Epilepsy and Behavior, 111. https://doi.org/10.1016/j.yebeh.2020.107370
Tallarita, G. M., Parente, A., & Giovagnoli, A. R. (2019). The visuospatial pattern of temporal lobe epilepsy. Epilepsy and Behavior, 101. https://doi.org/10.1016/j.yebeh.2019.106582
Téllez-Zenteno, J. F., & Hernández-Ronquillo, L. (2012). A Review of the Epidemiology of Temporal Lobe Epilepsy. Epilepsy Research and Treatment, 2012, 1–5. https://doi.org/10.1155/2012/630853
Tsuda, K., Tsuji, T., Ishida, T., Takahashi, S., Yamada, S., Ohoshi, Y., et al. (2018). Widespread abnormalities in white matter integrity and their relationship with duration of illness in temporal lobe epilepsy. Epilepsia Open, 3(2), 247–254. https://doi.org/10.1002/epi4.12222
Wang, H., Huang, Y., Coman, D., Munbodh, R., Dhaher, R., Zaveri, H. P., et al. (2017). Network evolution in mesial temporal lobe epilepsy revealed by diffusion tensor imaging. Epilepsia, 58(5), 824–834. https://doi.org/10.1111/epi.13731
Whelan, C. D., Altmann, A., Botía, J. A., Jahanshad, N., Hibar, D. P., Absil, J., et al. (2018). Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain, 141(2), 391–408. https://doi.org/10.1093/brain/awx341
Acknowledgements
The authors thank Celine Cavallo for English language support.
Funding
This study was supported by a predoctoral grant in Neuroscience by Fundación Tatiana Pérez de Guzmán el Bueno. This funding source was not involved in the study design, collection, analysis or interpretation of the data, writing of the report, or submission for publication.
Author information
Authors and Affiliations
Contributions
Author contributions included conception and study design (EF, SS, DP and MT), data collection or acquisition (EF, SS, DP, ES, LA and CT), statistical analysis (EF and MQ), interpretation of results (EF, MQ, SS and DP), drafting the manuscript work or revising it critically for important intellectual content (EF, SS, DP, MT, AR, MT) and approval of final version to be published and agreement to be accountable for the integrity and accuracy of all aspects of the work (all authors).
Corresponding author
Ethics declarations
Conflicts of interest
E. Fonseca declares research funding and honoraria from UCB Pharma, Esteve laboratorios, Eisai Inc, GW Pharmaceuticals, Angelini Pharma and Sanofi Genzyme. E. Santamarina declares research funding and speaking fees from UCB Pharma, BIAL Pharmaceutical, EISAI Inc. and Esteve laboratorios. L. Abraira declares research funding and speaking fees from UCB Pharma, BIAL Pharmaceutical, EISAI Inc., Sanofi Genzyme and Esteve laboratorios. I. Seijo declares research funding from UCB Pharma, Neuraxpharm and GW pharmaceuticals. M. Toledo declares research funding and speaking fees from UCB Pharma, BIAL Pharmaceutical, EISAI Inc., GW Pharmaceuticals, Arvelle Therapeutics, Angelini Pharma and Esteve laboratorios. S. Sarria, D. Pareto, M. Turon, M. Quintana, C. Tortajada and A. Rovira have no conflicts of interest to declare.
Ethics approval
We confirm that we have read the journal’s position on issues concerning ethical publication and that this report is consistent with those guidelines. The study protocol was approved by the Vall d’Hebron Research Institute Ethics Committee [PR(AG)391/2017], following the Ethics of the World Medical Association for experiments involving humans. The study conforms with the STROBE guidelines for observational studies.
Consent to participate
All patients provided signed written informed consent prior to inclusion in the study.
Consent for publication
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary material
Graphical visualization of some of the most representative correlations between cognitive performance and cortical thickness and WM volume in both left and right TLE patients groups. These graphs show worse cognitive performance in TLE patients with lower cortical thickness and lower WM volume. JLO, Judgement of line orientation test; ROCF-DR, delayed recall of the Rey-Osterrieth complex figure; ROCF-IR, immediate recall of the Rey-Osterrieth complex figure; TLE, temporal lobe epilepsy; VOT, Hooper visual organization test; WM, white matter (PNG 558 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Fonseca, E., Sarria-Estrada, S., Pareto, D. et al. Relationship between visuoperceptual functions and parietal structural abnormalities in temporal lobe epilepsy. Brain Imaging and Behavior 17, 35–43 (2023). https://doi.org/10.1007/s11682-022-00738-2
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-022-00738-2