Skip to main content

Advertisement

SpringerLink
Log in

Preoperative neuropsychological presentation of patients with refractory frontal lobe epilepsy

  • Experimental Research - Neurosurgical Anatomy
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

This study investigated whether certain cognitive deficits are associated with frontal lobe epilepsy (FLE) aiming to contribute with localization data to the preoperative assessment of epilepsy surgery candidates.

Methods

We evaluated 34 patients with refractory FLE, 37 patients with refractory medial temporal lobe epilepsy (MTLE), and 22 healthy individuals in attention, psychomotor speed, motor function, verbal memory span, verbal fluency, response inhibition/interference, concept formation and set shifting, anticipation and planning, global memory.

Results

Neuropsychological performances of FLE and MTLE were similar, with the only exception the WCST-number of categories index, measuring mental flexibility, in which MTLE patients performed significantly worse than FLE patients. Left-FLE patients presented more perseverative responding compared to both other patient groups and healthy controls (HCs), while left-MTLE patients showed worse sorting abilities than the other epilepsy groups.

Conclusions

Our findings suggest a weak cognitive differentiation between FLE and MTLE, probably attributed to the intricate nature of fronto-temporal connectivity frequently resulting in overlapping deficits as well as the confounding effects of seizure-related variables. In clinical practice, a highly individualized (idiographic) neuropsychological approach along with the inclusion of concurrent EEG recordings (e.g., interictal coupling) may be of help for neuropsychologists in identifying FLE patients from those with medial temporal pathology presenting frontal dysfunction as a secondary cognitive symptom.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Manford M, Hart YM, Sander JW, Shorvon SD (1992) National General Practice Study of Epilepsy (NGPSE): partial seizure patterns in a general population. Neurology 42:1911–1917

    Article  CAS  PubMed  Google Scholar 

  2. Waterman K, Wada J (1990) Frontal lobe epilepsy. In: Dam M, Gram L (eds) Comprehensive epileptolo. Raven Pres, New York, pp 197–213

    Google Scholar 

  3. Helmstaedter C, Kemper B, Elger CE (1996) Neuropsychological aspects of frontal lobe epilepsy. Neuropsychologia 34:399–406

    Article  CAS  PubMed  Google Scholar 

  4. Hermann B, Seidenberg M, Lee EJ, Chan FM, Rutecki P (2007) Cognitive phenotypes in temporal lobe epilepsy. J Int Neuropsychol Soc 13:12–20

    Article  PubMed  Google Scholar 

  5. Delaney DC, Rosen AJ, Mattson RH, Novelly RA (1980) Memory function in focal epilepsy: a comparison of non surgical, unilateral temporal lobe and frontal lobe sample. Cortex 16:103–117

    Article  CAS  PubMed  Google Scholar 

  6. Drane D, Lee GP, Cech H, Huthwaite JS, Ojemann GA, Ojemann JG, Loring DW, Meador KJ (2006) Structured cueing on a semantic fluency task differentiates patients with temporal versus frontal lobe seizure onset. Epilepsy Behav 9:339–344

    Article  PubMed  PubMed Central  Google Scholar 

  7. Exner C, Boucsein K, Lange K, Winter H, Weniger G, Steinhoff BJ, Irle E (2002) Neuropsychological performance in frontal lobe epilepsy. Seizure 11:20–32

    Article  PubMed  Google Scholar 

  8. Farrant A, Morris RG, Russell T, Elwes R, Akanuma N, Alarcon G, Koutroumanidis M (2005) Social cognition in frontal lobe epilepsy. Epilepsy Behav 7:506–516

    Article  PubMed  Google Scholar 

  9. Giovagnoli AR (2001) Relation of sorting impairment to hippocampal damage in temporal lobe epilepsy. Neuropsychologia 39:140–150

    Article  CAS  PubMed  Google Scholar 

  10. Giovagnoli AR, Franceschetti S, Reati F et al (2011) Theory of mind in frontal and temporal lobe epilepsy: cognitive and neural aspects. Epilepsia 52(11):1995–2002

    Article  PubMed  Google Scholar 

  11. Kemper B, Helmstaedter C, Elger CE (1993) Neuropsychological assessment in patients with frontal lobe epilepsy. Epilepsia 34:170

    Google Scholar 

  12. McDonald CR, Delis DC, Norman MA, Wetter SR, Tecoma ES, Iragui VJ (2005) Response inhibition and set shifting in patients with frontal lobe epilepsy or temporal lobe epilepsy. Epilepsy Behav 7:438–46

    Article  PubMed  Google Scholar 

  13. McDonald CR, Delis DC, Kramer JH, Tecoma S, Iragui VJ (2008) A componential analysis of proverb interpretation in patients with frontal lobe epilepsy and temporal lobe epilepsy: relationships with disease-related factors. Clin Neuropsychol 22:1–17

    Article  Google Scholar 

  14. McDonald CR, Delis DC (2005) Discriminating patients with frontal-lobe epilepsy and temporal-lobe epilepsy: utility of a multilevel design fluency test. Neuropsychology 19:806–813

    Article  PubMed  Google Scholar 

  15. Milner B (1975) Psychological aspects of focal epilepsy and its neurosurgical management. In: Purpura DP, Walter RD (eds) Advances in neurology. Oxford Univ. Press, New York, pp 299–321

    Google Scholar 

  16. Upton D, Thompson PJ (1996) General neuropsychological characteristics of frontal lobe epilepsy. Epilepsy Res 23:169–177

    Article  CAS  PubMed  Google Scholar 

  17. Upton D, Thompson PJ (1996) Epilepsy in the frontal lobes: neuropsychological characteristics. J Epilepsy 9:215–222

    Article  Google Scholar 

  18. Patrikelis P, Angelakis E, Gatzonis S (2009) Neurocognitive and behavioral functioning in frontal lobe epilepsy: a review. Epilepsy Behav 14:19–26

    Article  PubMed  Google Scholar 

  19. Horner MD, Flashman LA, Freides D, Epstein CM, Bakay RA (1996) Temporal lobe epilepsy and performance on the Wisconsin Card Sorting Test. J Clin Exp Neuropsychol 18:310–313

    Article  CAS  PubMed  Google Scholar 

  20. Hermann BP, Wyler AR, Richley ET (1988) Wisconsin Card Sorting Test performance in patients with complex partial seizures of temporal lobe origin. J Clin Exp Neuropsychol 10:467–476

    Article  CAS  PubMed  Google Scholar 

  21. Jokeit H, Schacher M (2004) Neuropsychological aspects of type of epilepsy and etiological factors in adults. Epilepsy Behav 5:14–20

    Article  Google Scholar 

  22. (39)Mesulam, M M (1985) Patterns in behavioural neuroanatomy: Association areas, the limbic system, and hemispheric specialization. In M M Mesulam (eds) Behavioral Neurology Philadelphia: F.A. Davis Company, pp 1–70

  23. Kwan P, Arzimanoglou A, Berg AT, Brodie J, Hauser WA, Mathern G, Moshe’ SL, Perucca E, Wiebe S, French J (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

    Article  CAS  PubMed  Google Scholar 

  24. Kokkevi A, Repapi M, Adamou N, Stefanis C (1979) Adjustment and standardization of WAIS in Greek population (in Greek). Iatriki 35:512–518

    Google Scholar 

  25. Wechsler D (1955) Wechsler Adult Intelligence Scale. The Psychological Corporation, New York

    Google Scholar 

  26. Dicksteina LS, Blatta SJ (1967) The WAIS Picture Arrangement Subtest as a measure of anticipation. J Proj Tech Pers Assess 31:32–38

    Google Scholar 

  27. Lezak MD (1995) Neuropsychological assessment, 3rd edn. Oxford University Press, New York

    Google Scholar 

  28. Strauss, E, Sherman E M S, Spreen, O (2006) A compendium of neuropsychological tests: administration, norms, and commentary, (third eds) New York: Oxford University Press pp, 760–769

  29. Wilson BA, Clare I, Baddeley AD, Cockburn J, Watson P, Tate R (1999) The Rivermead Behavioural Memory Test-Extended Version. Thames Valley Test Company, Bury St. Edmunds

    Google Scholar 

  30. Partington JE, Leiter RG (1949) Partington’s pathway test. Psychol Serv Center Bull 1:9–20

    Google Scholar 

  31. Zalonis I, Kararizou E, Triantafyllou NI, Kapaki E, Papageorgiou S, Sgouropoulos P, Vasilopoulos D (2008) A normative study of the Trail Making Test A and B in Greek adults. Clin Neuropsychol 22:842–850

    Article  CAS  PubMed  Google Scholar 

  32. Zalonis I, Christidi F, Bonakis A, Kararizou E, Triantafyllou NI, Paraskevas G, Kapaki E, Vasilopoulos D (2009) The Stroop effect in Greek healthy population: Normative data for the Stroop Neuropsychological Screening Test. Arch Clin Neuropsychol 24:81–88

    Article  PubMed  Google Scholar 

  33. Kongs SK, Thompson LL, Iverson GL, Heaton RK (2000) WCST-64: Wisconsin Card Sorting Test-64 card version, professional manual. Psychological Assessment Resources, Odessa

    Google Scholar 

  34. Baldo JV, Shimamura AP (1998) Letter and category fluency in patients with frontal lobe lesions. Neuropsychology 12(2):259–267

    Article  CAS  PubMed  Google Scholar 

  35. Benton, A L, Hamsher, K, Sivan, A B (1994) Multilingual Aphasia Examination (3rd ed) AJA Associates, Iowa City IA

  36. Kosmidis MH, Vlahou CH, Panagiotaki P, Kiosseoglou G (2004) The verbal fluency task in the Greek population: normative data, and clustering and switching strategies. J Int Neuropsychol Soc 10:164–172

    PubMed  Google Scholar 

  37. Elger CE, Helmstaedter C, Kurthen M (2004) Chronic epilepsy and cognition. Lancet Neurol 3:663–672

    Article  PubMed  Google Scholar 

  38. Segalowitz SJ, Unsal A, Dywan J (1992) CNV evidence for the distinctiveness of frontal and posterior neural processes in a traumatic brain injury population. J Clin Exp Neuropsychol 14:545–565

    Article  CAS  PubMed  Google Scholar 

  39. Zakzanis KK, Mrazb R, Graham SJ (2005) An fMRI study of the Trail Making Test. Neuropsychologia 43:1878–1886

    Article  PubMed  Google Scholar 

  40. Bornstein RA (1986) Contribution of various neuropsychological measures to detection of frontal lobe impairment. Int J Clin Neuropsychol 8:18–22

    Google Scholar 

  41. Milner B (1963) Effects of different brain lesions on card sorting. Arch Neurol 9:90–100

    Article  Google Scholar 

  42. Konishi S, Hayashi T, Uchida I, Kikyo H, Takahashi E, Miyashita Y (2002) Hemispheric asymmetry in human lateral prefrontal cortex during cognitive set shifting. Proc Natl Acad Sci 99:7803–7808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lieb JP, Dasheiff RM, Engel J (1991) Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia 32:8228–8237

    Article  Google Scholar 

  44. Stretton J, Thompson PJ (2011) Frontal lobes function in temporal lobe epilepsy. Epilepsy Res 98:1–13

    Article  PubMed  Google Scholar 

  45. Upton D, Thompson PJ (1997) Neuropsychological test performance in frontal-lobe epilepsy: the influence of aetiology, seizure type, seizure frequency and duration of disorder. Seizure 6:443–447

    Article  CAS  PubMed  Google Scholar 

  46. Strauss E, Loring D, Chelune G, Hunter M, Hermann BP, Perrine K, Westerveld M, Trenerry M, Barr W (1995) Predicting cognitive impairment in epilepsy: findings from the Bozeman epilepsy consortium. J Clin Exp Neuropsychol 17(6):909–917

    Article  CAS  PubMed  Google Scholar 

  47. Lüders H (1991) Epilepsy surgery. Raven Press, New York

    Google Scholar 

  48. Zamarian, L, Trinka, E, Bonatti, E, Kuchukhidze, G, Bodner, T, Benke, T, Koppelstaetter, F, Delazer, M (2011) Executive functions in chronic mesial temporal lobe epilepsy. Epilepsy Research and Treatment 1–11

  49. Saling MM (2009) Verbal memory in mesial temporal lobe epilepsy: beyond material specificity. Brain 132:570–582

    Article  PubMed  Google Scholar 

  50. Glikmann-Johnston Y, Saling MM, Reutens DC (2008) Structural and functional correlates of unilateral mesial temporal spatial memory impairment. Brain 131(11):3006–3018

    Article  PubMed  Google Scholar 

  51. McConley R, Martin R, Palmer CA, Kuzniecky R, Knowlton R, Faught E (2008) Rey Osterrieth complex figure test spatial and figural scoring: relations to seizure focus and hippocampal pathology in patients with temporal lobe epilepsy. Epilepsy Behav 13(1):174–177

    Article  PubMed  Google Scholar 

  52. Kennepohl S, Sziklas V, Garver KE, Wagner DD, Jones-Gotman M (2007) Memory and the medial temporal lobe: hemispheric specialization reconsidered. NeuroImage 36(3):969–978

    Article  CAS  PubMed  Google Scholar 

  53. Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial episodic memory. Neuron 35(4):625–641

    Article  CAS  PubMed  Google Scholar 

  54. Law JR, Flanery MA, Wirth S, Yanilke M, Smith AC, Frank LM et al (2005) Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory. J Neurosci 25(4):5720–5729

    Article  CAS  PubMed  Google Scholar 

  55. Nyberg L, Persson J, Habib R, Tulving E, McIntosh AR, Cabeza R et al (2000) Large scale neurocognitive networks underlying episodic memory. J Cogn Neurosci 12(1):163–173

    Article  CAS  PubMed  Google Scholar 

  56. Sommer T, Rose M, Glascher J, Wolbers T, Buchel C (2005) Dissociable contributions within the medial temporal lobe to encoding of objectlocation associations. Learn Mem 12(1):343–351

    Article  PubMed  PubMed Central  Google Scholar 

  57. Treyer V, Buck A, Schnider A (2005) Processing content or location: Distinct brain activation in a memory task. Hippocampus 15(5):684–689

    Article  PubMed  Google Scholar 

  58. Luria AR (1966) Higehr cortical functions in man. Basic Books, New York

    Google Scholar 

  59. Pillon B, Bazin B, Deweer B et al (1999) Specificity of memory deficits after right or left temporal lobectomy. Cortex 35(4):561–571

    Article  CAS  PubMed  Google Scholar 

  60. Baxendale S, Thompson P (2010) Beyond localization: the role of traditional neuropsychological tests in an age of imaging. Epilepsia 51(11):2225–2230

  61. Loring DW, Meador KJ, Lee GP, Smith JR (2004) Structural versus functional prediction of memory change following anterior temporal lobectomy. Epilepsy Behav 5(2):264–268

  62. Aldenkamp AP, Arend J (2004) Effects of epileptiform EEG discharges on cognitive function: Is the concept of “transient cognitive impairment” still valid? Epilepsy Behav 5(Sup1):25–34

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Epilepsy Surgery Unit, School of Medicine, University of Athens, Evangelismos Hospital, 45-47 Ipsilantou Str., 10676, Athens, Greece

    Panayiotis Patrikelis, Stylianos Gatzonis, Anna Siatouni, Maria Takousi & Damianos E. Sakas

  2. First Department of Psychiatry, School of Medicine, University of Athens, Eginition Hospital, 11528, Athens, Greece

    Elias Angelopoulos & George Konstantakopoulos

  3. Section of Cognitive Neuropsychiatry, Institute of Psychiatry, King’s College London, SE58AF, London, UK

    George Konstantakopoulos

  4. Department of Neurology, School of Medicine, University of Athens, Eginition Hospital, 11528, Athens, Greece

    Ioannis Zalonis

Authors
  1. Panayiotis Patrikelis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stylianos Gatzonis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anna Siatouni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elias Angelopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. George Konstantakopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Takousi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Damianos E. Sakas
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ioannis Zalonis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Panayiotis Patrikelis.

Ethics declarations

Funding

No funding was received for this research.

Conflict of Interest

None.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Patrikelis, P., Gatzonis, S., Siatouni, A. et al. Preoperative neuropsychological presentation of patients with refractory frontal lobe epilepsy. Acta Neurochir 158, 1139–1150 (2016). https://doi.org/10.1007/s00701-016-2786-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-016-2786-4

Keywords

Search

Navigation