Stereoelectroencephalographic language mapping of the basal temporal cortex predicts postoperative naming outcome

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  • 1 Departments of Neurology and
  • 2 Neurosurgery, University Hospital of Nancy, Lorraine University, Nancy, France;
  • 3 Neurosciences of Systems and Cognition Project, BioSiS Department (Department Biologie, Signaux et Systèmes en Cancérologie et Neurosciences), Research Center for Automatic Control of Nancy (CRAN), Lorraine University, CNRS, UMR 7039, Vandoeuvre, France; and
  • 4 Neurology and Neurosurgery Department, Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada
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OBJECTIVE

In drug-resistant temporal lobe epilepsy (TLE) patients, the authors evaluated early and late outcomes for decline in visual object naming after dominant temporal lobe resection (TLR) according to the resection status of the basal temporal language area (BTLA) identified by cortical stimulation during stereoelectroencephalography (SEEG).

METHODS

Twenty patients who underwent SEEG for drug-resistant TLE met the inclusion criteria. During language mapping, a site was considered positive when stimulation of two contiguous contacts elicited at least one naming impairment during two remote sessions. After TLR ipsilateral to their BTLA, patients were classified as BTLA+ when at least one positive language site was resected and as BTLA− when all positive language sites were preserved. Outcomes in naming and verbal fluency tests were assessed using pre- and postoperative (means of 7 and 25 months after surgery) scores at the group level and reliable change indices (RCIs) for clinically meaningful changes at the individual level.

RESULTS

BTLA+ patients (n = 7) had significantly worse naming scores than BTLA− patients (n = 13) within 1 year after surgery but not at the long-term evaluation. No difference in verbal fluency tests was observed. When RCIs were used, 5 of 18 patients (28%) had naming decline within 1 year postoperatively (corresponding to 57% of BTLA+ and 9% of BTLA− patients). A significant correlation was found between BTLA resection and naming decline.

CONCLUSIONS

BTLA resection is associated with a specific and early naming decline. Even if this decline is transient, naming scores in BTLA+ patients tend to remain lower compared to their baseline. SEEG mapping helps to predict postoperative language outcome after dominant TLR.

ABBREVIATIONS AH = amygdalo-hippocampal complex; BTLA = basal temporal language area; BTLA+ = resected BTLA; BTLA− = nonresected BTLA; DO80 = Dénomination Orale d’images 80; EZ = epileptogenic zone; FG = fusiform gyrus; HS = hippocampal sclerosis; ITG = inferior temporal gyrus; MTG = middle temporal gyrus; OTS = occipito-temporal sulcus; PHG = parahippocampal gyrus; RCI = reliable change index; SEEG = stereoelectroencephalography; SQRT = square root transformation; STG = superior temporal gyrus; TLE = temporal lobe epilepsy; TLR = temporal lobe resection; T1 = baseline assessment; T2 = early postoperative assessment; T3 = late postoperative assessment.

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Contributor Notes

Correspondence Louis Maillard: Lorraine University, Nancy, France. l.maillard@chru-nancy.fr.

INCLUDE WHEN CITING Published online February 26, 2021; DOI: 10.3171/2020.8.JNS202431.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

  • 1

    Spencer S, Huh L. Outcomes of epilepsy surgery in adults and children. Lancet Neurol. 2008;7(6):525537.

  • 2

    Maillard L, Vignal J-P, Gavaret M, Semiologic and electrophysiologic correlations in temporal lobe seizure subtypes. Epilepsia. 2004;45(12):15901599.

    • Search Google Scholar
    • Export Citation
  • 3

    Sherman EMS, Wiebe S, Fay-McClymont TB, Neuropsychological outcomes after epilepsy surgery: systematic review and pooled estimates. Epilepsia. 2011;52(5):857869.

    • Search Google Scholar
    • Export Citation
  • 4

    Busch RM, Hogue O, Kattan MW, Nomograms to predict naming decline after temporal lobe surgery in adults with epilepsy. Neurology. 2018;91(23):e2144e2152.

    • Search Google Scholar
    • Export Citation
  • 5

    Ives-Deliperi VL, Butler JT. Naming outcomes of anterior temporal lobectomy in epilepsy patients: a systematic review of the literature. Epilepsy Behav. 2012;24(2):194198.

    • Search Google Scholar
    • Export Citation
  • 6

    Ives-Deliperi V, Butler JT. Quality of life one year after epilepsy surgery. Epilepsy Behav. 2017;75:213217.

  • 7

    Stafiniak P, Saykin AJ, Sperling MR, Acute naming deficits following dominant temporal lobectomy: prediction by age at 1st risk for seizures. Neurology. 1990;40(10):15091512.

    • Search Google Scholar
    • Export Citation
  • 8

    Davies KG, Bell BD, Bush AJ, Naming decline after left anterior temporal lobectomy correlates with pathological status of resected hippocampus. Epilepsia. 1998;39(4):407419.

    • Search Google Scholar
    • Export Citation
  • 9

    Bell BD, Davies KG, Hermann BP, Walters G. Confrontation naming after anterior temporal lobectomy is related to age of acquisition of the object names. Neuropsychologia. 2000;38(1):8392.

    • Search Google Scholar
    • Export Citation
  • 10

    Schwarz M, Pauli E, Stefan H. Model based prognosis of postoperative object naming in left temporal lobe epilepsy. Seizure. 2005;14(8):562568.

    • Search Google Scholar
    • Export Citation
  • 11

    Hamberger MJ, Seidel WT, Goodman RR, Evidence for cortical reorganization of language in patients with hippocampal sclerosis. Brain. 2007;130(Pt 11):29422950.

    • Search Google Scholar
    • Export Citation
  • 12

    Hamberger MJ, Seidel WT, Goodman RR, McKhann GM II. Does cortical mapping protect naming if surgery includes hippocampal resection? Ann Neurol. 2010;67(3):345352.

    • Search Google Scholar
    • Export Citation
  • 13

    Yucus CJ, Tranel D. Preserved proper naming following left anterior temporal lobectomy is associated with early age of seizure onset. Epilepsia. 2007;48(12):22412252.

    • Search Google Scholar
    • Export Citation
  • 14

    Lüders H, Lesser RP, Hahn J, Basal temporal language area demonstrated by electrical stimulation. Neurology. 1986;36(4):505510.

  • 15

    Lüders H, Lesser RP, Hahn J, Basal temporal language area. Brain. 1991;114(Pt 2):743754.

  • 16

    Burnstine TH, Lesser RP, Hart J Jr, Characterization of the basal temporal language area in patients with left temporal lobe epilepsy. Neurology. 1990;40(6):966970.

    • Search Google Scholar
    • Export Citation
  • 17

    Bédos Ulvin L, Jonas J, Brissart H, Intracerebral stimulation of left and right ventral temporal cortex during object naming. Brain Lang. 2017;175(October):7176.

    • Search Google Scholar
    • Export Citation
  • 18

    Krauss GL, Fisher R, Plate C, Cognitive effects of resecting basal temporal language areas. Epilepsia. 1996;37(5):476483.

  • 19

    Jonas J, Maillard L, Frismand S, Self-face hallucination evoked by electrical stimulation of the human brain. Neurology. 2014;83(4):336338.

    • Search Google Scholar
    • Export Citation
  • 20

    Deloche G, Hannequin D. Test de dénomination orale d’images. Centre de Psychologie Appliquée; 1997.

  • 21

    Godefroy O. Fonctions exécutives et pathologies neurologiques et psychiatriques: évaluation en pratique clinique. Solal; 2008.

  • 22

    Isnard J, Taussig D, Bartolomei F, French guidelines on stereoelectroencephalography (SEEG). Neurophysiol Clin. 2018;48(1):513.

  • 23

    Bancaud J, Talairach J. Methodology of stereo EEG exploration and surgical intervention in epilepsy. Article in French. Rev Otoneuroophtalmol. 1973;45(4):315328.

    • Search Google Scholar
    • Export Citation
  • 24

    Maillard LG, Tassi L, Bartolomei F, Stereoelectroencephalography and surgical outcome in polymicrogyria-related epilepsy: a multicentric study. Ann Neurol. 2017;82(5):781794.

    • Search Google Scholar
    • Export Citation
  • 25

    Jonas J, Rossion B, Brissart H, Beyond the core face-processing network: intracerebral stimulation of a face-selective area in the right anterior fusiform gyrus elicits transient prosopagnosia. Cortex. 2015;72:140155.

    • Search Google Scholar
    • Export Citation
  • 26

    Salado AL, Koessler L, De Mijolla G, sEEG is a safe procedure for a comprehensive anatomic exploration of the insula: a retrospective study of 108 procedures representing 254 transopercular insular electrodes. Oper Neurosurg (Hagerstown). 2018;14(1):18.

    • Search Google Scholar
    • Export Citation
  • 27

    Lancaster JL, Woldorff MG, Parsons LM, Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp. 2000;10(3):120131.

    • Search Google Scholar
    • Export Citation
  • 28

    Engel J Jr. Outcome with respect to epileptic seizures. In: Surgical Treatment of the Epilepsies. Raven Press; 1993.

  • 29

    Jacobson NS, Truax P. Clinical significance: a statistical approach to defining meaningful change in psychotherapy research. J Consult Clin Psychol. 1991;59(1):1219.

    • Search Google Scholar
    • Export Citation
  • 30

    Hermann BP, Seidenberg M, Schoenfeld J, Empirical techniques for determining the reliability, magnitude, and pattern of neuropsychological change after epilepsy surgery. Epilepsia. 1996;37(10):942950.

    • Search Google Scholar
    • Export Citation
  • 31

    Schäffler L, Lüders HO, Morris HH III, Wyllie E. Anatomic distribution of cortical language sites in the basal temporal language area in patients with left temporal lobe epilepsy. Epilepsia. 1994;35(3):525528.

    • Search Google Scholar
    • Export Citation
  • 32

    Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg. 1989;71(3):316326.

    • Search Google Scholar
    • Export Citation
  • 33

    Davies KG, Risse GL, Gates JR. Naming ability after tailored left temporal resection with extraoperative language mapping: increased risk of decline with later epilepsy onset age. Epilepsy Behav. 2005;7(2):273278.

    • Search Google Scholar
    • Export Citation
  • 34

    Giovagnoli AR, Parente A, Didato G, The course of language functions after temporal lobe epilepsy surgery: a prospective study. Eur J Neurol. 2016;23(12):17131721.

    • Search Google Scholar
    • Export Citation
  • 35

    Engel J Jr, McDermott MP, Wiebe S, Early surgical therapy for drug-resistant temporal lobe epilepsy: a randomized trial. JAMA. 2012;307(9):922930.

    • Search Google Scholar
    • Export Citation
  • 36

    Hill SW, Gale SD, Pearson C, Smith K. Neuropsychological outcome following minimal access subtemporal selective amygdalohippocampectomy. Seizure. 2012;21(5):353360.

    • Search Google Scholar
    • Export Citation
  • 37

    Busch RM, Floden DP, Prayson B, Estimating risk of word-finding problems in adults undergoing epilepsy surgery. Neurology. 2016;87(22):23632369.

    • Search Google Scholar
    • Export Citation
  • 38

    Schwarz M, Pauli E. Postoperative speech processing in temporal lobe epilepsy: functional relationship between object naming, semantics and phonology. Epilepsy Behav. 2009;16(4):629633.

    • Search Google Scholar
    • Export Citation
  • 39

    Bartha L, Trinka E, Ortler M, Linguistic deficits following left selective amygdalohippocampectomy: a prospective study. Epilepsy Behav. 2004;5(3):348357.

    • Search Google Scholar
    • Export Citation
  • 40

    Saykin AJ, Stafiniak P, Robinson LJ, Language before and after temporal lobectomy: specificity of acute changes and relation to early risk factors. Epilepsia. 1995;36(11):10711077.

    • Search Google Scholar
    • Export Citation

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