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Impaired Behavioral Pattern Separation in Refractory Temporal Lobe Epilepsy and Mild Cognitive Impairment

Published online by Cambridge University Press:  03 June 2021

Sanam J. Lalani Open the ORCID record for Sanam J. Lalani [Opens in a new window] ,
Anny Reyes ,
Erik Kaestner ,
Shauna M. Stark ,
Craig E.L. Stark ,
David Lee ,
Leena Kansal ,
Jerry J. Shih ,
Christine N. Smith  and
Brianna M. Paul
...Show all authors
Sanam J. Lalani
Affiliation:
Department of Neurology, University of California San Francisco, San Francisco, CA, USA
Anny Reyes
Affiliation:
San Diego State University, University of California San Diego Joint Doctoral Program in Clinical Psychology, San Diego, CA, USA Center for Multimodal Imaging and Genetics, University of California, San Diego, CA, USA Department of Psychiatry, University of California, San Diego, CA, USA
Erik Kaestner
Affiliation:
Center for Multimodal Imaging and Genetics, University of California, San Diego, CA, USA Department of Psychiatry, University of California, San Diego, CA, USA
Shauna M. Stark
Affiliation:
Department of Neurobiology and Behavior, University of California Irvine, Irvine, CA, USA
Craig E.L. Stark
Affiliation:
Department of Neurobiology and Behavior, University of California Irvine, Irvine, CA, USA
David Lee
Affiliation:
Department of Neurosciences, University of California San Diego, San Diego, CA, USA
Leena Kansal
Affiliation:
Department of Neurosciences, University of California San Diego, San Diego, CA, USA
Jerry J. Shih
Affiliation:
Department of Neurosciences, University of California San Diego, San Diego, CA, USA
Christine N. Smith
Affiliation:
Department of Psychiatry, University of California, San Diego, CA, USA Veterans Affairs San Diego Healthcare System, San Diego, CA, USA Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, CA, USA
Brianna M. Paul
Affiliation:
Department of Neurology, University of California San Francisco, San Francisco, CA, USA
Carrie R. McDonald*
Affiliation:
San Diego State University, University of California San Diego Joint Doctoral Program in Clinical Psychology, San Diego, CA, USA Center for Multimodal Imaging and Genetics, University of California, San Diego, CA, USA Department of Psychiatry, University of California, San Diego, CA, USA
*
*Correspondence and reprint requests to: Carrie R. McDonald, 8950 Villa La Jolla Drive, Multimodal Imaging Laboratory (Suite C101), La Jolla, CA92037, USA. Email: [email protected]
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Abstract

Objective:

Episodic memory impairment and hippocampal pathology are hallmark features of both temporal lobe epilepsy (TLE) and amnestic mild cognitive impairment (aMCI). Pattern separation (PS), which enables the distinction between similar but unique experiences, is thought to contribute to successful encoding and retrieval of episodic memories. Impaired PS has been proposed as a potential mechanism underling episodic memory impairment in aMCI, but this association is less established in TLE. In this study, we examined behavioral PS in patients with TLE and explored whether profiles of performance in TLE are similar to aMCI.

Method:

Patients with TLE, aMCI, and age-matched, healthy controls (HCs) completed a modified recognition task that relies on PS for the discrimination of highly similar lure items, the Mnemonic Similarity Task (MST). Group differences were evaluated and relationships between clinical characteristics, California Verbal Learning Test—Second Edition scores, and MST performance were tested in the TLE group.

Results:

Patients with TLE and aMCI demonstrated poorer PS performance relative to the HCs, but performance did not differ between the two patient groups. Neither the side of seizure focus nor having hippocampal sclerosis affected performance in TLE. However, TLE patients with clinically defined memory impairment showed the poorest performance.

Conclusion:

Memory performance on a task that relies on PS was disrupted to a similar extent in TLE and aMCI. The MST could provide a clinically useful tool for measuring hippocampus-dependent memory impairments in TLE and other neurological disorders associated with hippocampal damage.

Keywords

Episodic memoryMemory impairmentCognitionHippocampusAgingSeizure disorder
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 28 , Issue 6 , July 2022 , pp. 550 - 562
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

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References

REFERENCES

Baker, S., Vieweg, P., Gao, F., Gilboa, A., Wolbers, T., Black, S.E., & Rosenbaum, R.S. (2016). The human dentate gyrus plays a necessary role in discriminating new memories. Current Biology, 26(19), 2629–2634.CrossRefGoogle Scholar
Bakker, A., Albert, M.S., Krauss, G., Speck, C.L., & Gallagher, M. (2015). Response of the medial temporal lobe network in amnestic mild cognitive impairment to therapeutic intervention assessed by fMRI and memory task performance. NeuroImage: Clinical, 7, 688–698.CrossRefGoogle ScholarPubMed
Bakker, A., Kirwan, C.B., Miller, M., & Stark, C.E.L. (2008). Pattern separation in the human hippocampal CA3 and dentate gyrus. Science, 319(5870), 1640–1642. https://doi.org/10.1126/science.1152882 CrossRefGoogle ScholarPubMed
Bakker, A., Krauss, G.L., Albert, M.S., Speck, C.L., Jones, L.R., Stark, C.E.L., … Gallagher, M. (2012). Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron, 74(3), 467–474. https://doi.org/10.1016/j.neuron.2012.03.023 CrossRefGoogle ScholarPubMed
Bell, B., Lin, J.J., Seidenberg, M., & Hermann, B.P. (2011). The neurobiology of cognitive disorders in temporal lobe epilepsy. Nature Reviews Neurology, 7(3), 154–164.CrossRefGoogle ScholarPubMed
Blumcke, I., Pauli, E., Clusmann, H., Schramm, J., Becker, A., Elger, C., … Hildebrandt, M. (2007). A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathology, 113(3), 235–244.CrossRefGoogle ScholarPubMed
Capraz, I.Y., Kurt, G., Akdemir, Ö., Hirfanoglu, T., Oner, Y., Sengezer, T., … Bilir, E. (2015). Surgical outcome in patients with MRI-negative, PET-positive temporal lobe epilepsy. Seizure, 29, 63–68.CrossRefGoogle ScholarPubMed
Cogstate. (2020). Computerized cognitive assessment: Guiding decision-making for safety and efficacy across indications and clinical trial phases. Retrieved from https://www.cogstate.com/clinical-trials/computerized-cognitive-assessment/ Google Scholar
Coras, R., Pauli, E., Li, J., Schwarz, M., Rössler, K., Buchfelder, M., … Blumcke, I. (2014). Differential influence of hippocampal subfields to memory formation: Insights from patients with temporal lobe epilepsy. Brain, 137(7), 1945–1957.CrossRefGoogle ScholarPubMed
Davidson, P.S., Vidjen, P., Trincao-Batra, S., & Collin, C.A. (2019). Older adults’ lure discrimination difficulties on the Mnemonic Similarity Task are significantly correlated with their visual perception. The Journals of Gerontology: Series B, 74(8), 1298–1307.CrossRefGoogle ScholarPubMed
De Flores, R., La Joie, R., & Chetelat, G. (2015). Structural imaging of hippocampal subfields in healthy aging and Alzheimer’s disease. Neuroscience, 309, 29–50.CrossRefGoogle Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A.. (2000). California Verbal Learning Test–Second Edition (CVLT-II). San Antonio, TX: The Psychological Corporation.Google Scholar
Doxey, C.R., & Kirwan, C.B. (2015). Structural and functional correlates of behavioral pattern separation in the hippocampus and medial temporal lobe. Hippocampus, 25(4), 524–533.CrossRefGoogle ScholarPubMed
Duff, M.C., Warren, D.E., Gupta, R., Vidal, J.P., Tranel, D., & Cohen, N.J. (2012). Teasing apart tangrams: Testing hippocampal pattern separation with a collaborative referencing paradigm. Hippocampus, 22(5), 1087–1091.CrossRefGoogle ScholarPubMed
Engel, J., Wiebe, S., French, J., Sperling, M., Williamson, P., Spencer, D., … Enos, B. (2003). Practice parameter: Temporal lobe and localized neocortical resections for Epilepsy. Epilepsia, 44(4), 741–751.CrossRefGoogle ScholarPubMed
Fisher, R.S., Cross, J.H., French, J.A., Higurashi, N., Hirsch, E., Jansen, F.E., … Zuberi, S. M. (2017). Operational classification of seizure types by the International League Against Epilepsy: Position paper of the ILAE commission for classification and terminology. Epilepsia, 58(4), 522–530.CrossRefGoogle ScholarPubMed
Foster, C.M., & Giovanello, K.S. (2020). Domain general processes moderate age-related performance differences on the mnemonic similarity task. Memory, 28(4), 528–536.CrossRefGoogle ScholarPubMed
Gainotti, G., Ferraccioli, M., Vita, M.G., & Marra, C. (2008). Patterns of neuropsychological impairment in MCI patients with small subcortical infarcts or hippocampal atrophy. Journal of the International Neuropsychological Society, 14(4), 611–619.CrossRefGoogle ScholarPubMed
Gilbert, P.E., Kesner, R.P., & DeCoteau, W.E. (1998). Memory for spatial location: Role of the hippocampus in mediating spatial pattern separation. The Journal of Neuroscience, 18(2), 804–810.CrossRefGoogle ScholarPubMed
Griffith, H.R., Martin, R.C., Bambara, J.K., Marson, D.C., & Faught, E. (2006). Older adults with epilepsy demonstrate cognitive impairments compared with patients with amnestic mild cognitive impairment. Epilepsy & Behavior, 8(1), 161–168.CrossRefGoogle ScholarPubMed
Hatanpaa, K.J., Raisanen, J.M., Herndon, E., Burns, D.K., Foong, C., Habib, A.A., & White, C.L. III (2014). Hippocampal sclerosis in dementia, epilepsy, and ischemic injury: Differential vulnerability of hippocampal subfields. Journal of Neuropathology & Experimental Neurology, 73(2), 136–142.CrossRefGoogle ScholarPubMed
Helmstaedter, C. (2013). Cognitive outcomes of different surgical approaches in temporal lobe epilepsy. Epileptic Disorders, 15(3), 221–239.Google ScholarPubMed
Hermann, B.P., Seidenberg, M., Schoenfeld, J., & Davies, K. (1997). Neuropsychological characteristics of the syndrome of mesial temporal lobe epilepsy. Archives of Neurology, 54, 369–376.CrossRefGoogle Scholar
Holden, H.M., Toner, C., Pirogovsky, E., Kirwan, C.B., & Gilbert, P.E. (2013). Visual object pattern separation varies in older adults. Learning & Memory, 20(7), 358–362.CrossRefGoogle ScholarPubMed
Huffman, D.J., & Stark, C.E. (2017). Age-related impairment on a forced-choice version of the Mnemonic Similarity Task. Behavioral Neuroscience, 131(1), 55–67.CrossRefGoogle ScholarPubMed
Hughes, C.P., Berg, L., Danziger, W., Coben, L.A., & Martin, R.L. (1982). A new clinical scale for the staging of dementia. The British Journal of Psychiatry, 140(6), 566–572.CrossRefGoogle ScholarPubMed
Kirwan, C.B., & Stark, C.E.L. (2007). Overcoming interference: An fMRI investigation of pattern separation in the medial temporal lobe. Learning and Memory, 14, 625–633.CrossRefGoogle Scholar
Kirwan, C.B., Hartshorn, A., Stark, S.M., Goodrich-Hunsaker, N.J., Hopkins, R.O., & Stark, C.E.L. (2012). Pattern separation deficits following damage to the hippocampus. Neuropsychologia, 50(10), 2408–2414.CrossRefGoogle Scholar
Koutstaal, W., & Schacter, D.L. (1997). Gist-based false recognition of pictures in older and younger adults. Journal of Memory and Language, 37(4), 555–583.CrossRefGoogle Scholar
Koutstaal, W., Schacter, D.L., Galluccio, L., & Stofer, K.A. (1999). Reducing gist-based false recognition in older adults: Encoding and retrieval manipulations. Psychology and Aging, 14(2), 220.CrossRefGoogle ScholarPubMed
Kraguljac, N.V., Carle, M., Frölich, M.A., Tran, S., Yassa, M.A., White, D.M., … Lahti, A. C. (2018). Mnemonic discrimination deficits in first-episode psychosis and a ketamine model suggests dentate gyrus pathology linked to N -methyl-D-aspartate receptor hypofunction. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3(3), 231–238.Google Scholar
Lacy, J.W., Yassa, M.A., Stark, S.M., Muftuler, L.T., & Stark, C.E.L. (2011). Distinct pattern separation related transfer functions in human CA1 and CA3/DG revealed using high-resolution fMRI and mnemonic similarity. Learning and Memory, 18, 15–18.CrossRefGoogle Scholar
Lapointe, E., Deacon, C., Royer-Perron, L., Cunnane, S., Castellano, C.A., & Bocti, C. (2016). Temporal lobe atrophy may be underrecognized in older patients with new-onset epilepsy. Journal of Neurological Sciences, 43(5), 731–734. https://doi.org/10.1017/cjn.2016.275 CrossRefGoogle ScholarPubMed
Leutgeb, J.K., Leutgeb, S., Moser, M.B., & Moser, E.I. (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science, 315(5814), 961–966. https://doi.org/10.1126/science.1135801 CrossRefGoogle ScholarPubMed
Leutgeb, S., Leutgeb, J.K., Treves, A., Moser, M., & Moser, E.I. (2004). Distinct ensemble codes in hippocampal areas CA3 and CA1. Science, 305(5688), 1295–1298.CrossRefGoogle ScholarPubMed
Martinelli, C., & Shergill, S.S. (2015). Clarifying the role of pattern separation in schizophrenia: The role of recognition and visual discrimination deficits. Schizophrenia Research, 166, 328–333.CrossRefGoogle ScholarPubMed
Motley, S.E., & Kirwan, C.B. (2012). A parametric investigation of pattern separation processes in the medial temporal lobe. Journal of Neuroscience, 32(38), 13076–13084.CrossRefGoogle ScholarPubMed
Mueller, S.G., Laxer, K.D., Scanlon, C., Garcia, P., McMullen, W.J., Loring, D.W., Meador, K.J., & Weiner, M.W. (2012). Different structural correlates for verbal memory impairment in temporal lobe epilepsy with and without mesial temporal lobe sclerosis. Human Brain Mapping, 33, 489–499.CrossRefGoogle ScholarPubMed
Mueller, S.G., Schuff, N., Yaffe, K., Madison, C., Miller, B., & Weiner, M.W. (2010). Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer’s disease. Human Brain Mapping, 31(9), 1339–1347.CrossRefGoogle ScholarPubMed
Nash, M.I., Hodges, C.B., Muncy, N.M., & Kirwan, C.B. (2021). Pattern separation beyond the hippocampus: A high-resolution whole-brain investigation of mnemonic discrimination in healthy adults. Hippocampus. Advance online publication. https://doi.org/10.1002/hipo.23299 CrossRefGoogle Scholar
Papp, K.V., Rentz, D.M., Maruff, P., Sun, C.-K., Raman, R., Donohue, M.C., … Sperling, R.A. (2020). The computerized cognitive composite (C3) in an Alzheimer’s disease secondary prevention trial. The Journal of Prevention of Alzheimer’s Disease, 8(1), 59–67.Google Scholar
Petersen, R.C. (2011). Mild cognitive impairment. New England Journal of Medicine, 364(23), 2227–2234.CrossRefGoogle ScholarPubMed
Petersen, R.C., Jack, C.R. Jr., Xu, Y.C., Waring, S.C., O’Brien, P.C., Smith, G.E., … Kokmen, E. (2000). Memory and MRI-based hippocampal volumes in aging and AD. Neurology, 54(3), 581–587. https://doi.org/10.1212/wnl.54.3.581 CrossRefGoogle ScholarPubMed
Petersen, R.C., Smith, G.E., Waring, S.C., Ivnik, R.J., Tangalos, E.G., & Kokmen, E. (1999). Mild cognitive impairment: Clinical characterization and outcome. Archives of Neurology, 56, 303–308.CrossRefGoogle Scholar
Pishdadian, S., Hoang, N.V., Baker, S., Moscovitch, M., & Rosenbaum, R.S. (2020). Not only memory: Investigating the sensitivity and specificity of the Mnemonic Similarity Task in older adults. Neuropsychologia, 149, 107670.CrossRefGoogle Scholar
Planche, V., Ruet, A., Charre-Morin, J., Deloire, M., Brochet, B., & Tourdias, T. (2017). Pattern separation performance is decreased in patients with early multiple sclerosis. Brain and Behavior, 7(8), e00739.CrossRefGoogle ScholarPubMed
Poch, C., Toledano, R., García-Morales, I., Prieto, A., García-Barragán, N., Aledo-Serrano, Á., Gil-Nagel, A., Campo, P. (2020). Mnemonic discrimination in patients with unilateral mesial temporal lobe epilepsy relates to similarity and number of events stored in memory. Neurobiology of Learning and Memory, 169, 107177.CrossRefGoogle Scholar
Reyes, A., Holden, H.M., Chang, Y.A., Uttarwar, V.S., Sheppard, D.P., DeFord, N.E., … McDonald, C. R. (2018). Impaired spatial pattern separation performance in temporal lobe epilepsy is associated with visuospatial memory deficits and hippocampal volume loss. Neuropsychologia, 111, 209–215.CrossRefGoogle Scholar
Rolls, E. (2013). The mechanisms for pattern completion and pattern separation in the hippocampus. Frontiers in Systems Neuroscience, 7, 74.CrossRefGoogle ScholarPubMed
Saling, M.M. (2009). Verbal memory in mesial temporal lobe epilepsy: Beyond material specificity. Brain, 132, 570–582.CrossRefGoogle Scholar
Schacter, D.L., Koutstaal, W., & Norman, K.A. (1997). False memories and aging. Trends in Cognitive Sciences, 1(6), 229–236.CrossRefGoogle ScholarPubMed
Schacter, D.L., Norman, K.A., & Koutstaal, W. (1998). The cognitive neuroscience of constructive memory. Annual Review of Psychology, 49(1), 289–318.CrossRefGoogle ScholarPubMed
Sen, A., Capelli, V., & Husain, M. (2018). Cognition and dementia in older patients with epilepsy. Brain, 141(6), 1592–1608. https://doi.org/10.1093/brain/awy022 CrossRefGoogle ScholarPubMed
Shiroma, A., Nishimura, M., Nagamine, H., Miyagi, T., Hokama, Y., Watanabe, T., … Ishiuchi, S. (2016). Cerebellar contribution to pattern separation of human hippocampal memory circuits. Cerebellum, 15(6), 645–662.CrossRefGoogle ScholarPubMed
South, M., Stephenson, K.G., Nielson, C.A., Maisel, M., Top, D.N., & Kirwan, C.B. (2015). Overactive pattern separation memory associated with negative emotionality in adults diagnosed with autism spectrum disorder. Journal of Autism and Developmental Disorders, 45(11), 3458–3467.CrossRefGoogle ScholarPubMed
Stark, S.M., Kirwan, C.B., & Stark, C.E.L. (2019). Mnemonic similarity task: A tool for assessing hippocampal integrity. Trends in Cognitive Sciences, 23(11), 938–951.CrossRefGoogle ScholarPubMed
Stark, S.M., & Stark, C.E. (2017). Age-related deficits in the mnemonic similarity task for objects and scenes. Behavioral Brain Research, 333, 109–117. https://doi.org/10.1016/j.bbr.2017.06.049 CrossRefGoogle ScholarPubMed
Stark, S.M., Stevenson, R., Wu, C., Rutledge, S., & Stark, C.E. (2015). Stability of age-related deficits in the mnemonic similarity task across task variations. Behavioral Neuroscience, 129(3), 257–268.CrossRefGoogle ScholarPubMed
Stark, S.M., Yassa, M.A., Lacy, J.W., & Stark, C.E. (2013). A task to assess behavioral pattern separation (BPS) in humans: Data from healthy aging and mild cognitive impairment. Neuropsychologia, 51(12), 2442–2449.CrossRefGoogle ScholarPubMed
Tai, X.Y., Bernhardt, B., Thom, M., Thompson, P., Baxendale, S., Koepp, M., & Bernasconi, N. (2018). Neurodegenerative processes in temporal lobe epilepsy with hippocampal sclerosis: Clinical, pathological and neuroimaging evidence. Neuropathology and Applied Neurobiology, 44(1), 70–90.CrossRefGoogle ScholarPubMed
Toner, C.K., Pirogovsky, E., Kirwan, C.B., & Gilbert, P.E. (2009). Visual object pattern separation deficits in nondemented older adults. Learning & Memory, 16(5), 338–342.CrossRefGoogle ScholarPubMed
Tulving, E. (2002). Episodic memory: From mind to brain. Annual Review of Psychology, 53(1), 1–25.CrossRefGoogle Scholar
Wais, P.E., Jahanikia, S., Steiner, D., Stark, C.E.L., & Gazzaley, A. (2017). Retrieval of high-fidelity memory arises from distributed cortical networks. NeuroImage, 149, 178–189.CrossRefGoogle ScholarPubMed
Wesnes, K.A., Annas, P., Basun, H., Edgar, C., & Blennow, K. (2014). Performance on a pattern separation task by Alzheimer’s patients shows possible links between disrupted dentate gyrus activity and apolipoprotein E ∈4 status and cerebrospinal fluid amyloid-β42 levels. Alzheimer’s Research & Therapy, 6(2), 1–8.Google ScholarPubMed
Yassa, M.A., & Stark, C.E.L. (2011). Pattern separation in the hippocampus. Trends in Neurosciences, 34(10), 515–525. https://doi.org/10.1016/j.tins.2011.06.006 CrossRefGoogle ScholarPubMed
Yassa, M.A., Stark, S.M., Bakker, A., Albert, M.S., Gallagher, M., & Stark, C.E.L. (2010). High-resolution structural and functional MRI of hippocampal CA3 and dentate gyrus in patients with amnestic mild cognitive impairment. NeuroImage, 51(3), 1242–1252. https://doi.org/10.1016/j.neuroimage.2010.03.040 CrossRefGoogle ScholarPubMed
Zuppichini, M.D., & Sandry, J. (2018). Pilot investigation of the relationship between hippocampal volume and pattern separation deficits in multiple sclerosis. Multiple Sclerosis and Related Disorders, 26, 157–163.CrossRefGoogle ScholarPubMed
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