Characterization of postsurgical functional connectivity changes in temporal lobe epilepsy

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  • 1 Vanderbilt University Institute of Imaging Science, Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center;
  • 2 Department of Biomedical Engineering, Vanderbilt University; and
  • 3 Department of Neurological Surgery, Vanderbilt University Medical Center, Nashville, Tennessee
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OBJECTIVE

Seizure outcome after mesial temporal lobe epilepsy (mTLE) surgery is complex and diverse, even across patients with homogeneous presurgical clinical profiles. The authors hypothesized that this is due in part to variations in network connectivity across the brain before and after surgery. Although presurgical network connectivity has been previously characterized in these patients, the objective of this study was to characterize presurgical to postsurgical functional network connectivity changes across the brain after mTLE surgery.

METHODS

Twenty patients with drug-refractory unilateral mTLE (5 left side, 10 female, age 39.3 ± 13.5 years) who underwent either selective amygdalohippocampectomy (n = 13) or temporal lobectomy (n = 7) were included in the study. Presurgical and postsurgical (36.6 ± 14.3 months after surgery) functional connectivity (FC) was measured with 3-T MRI and compared with findings in age-matched healthy controls (n = 44, 21 female, age 39.3 ± 14.3 years). Postsurgical connectivity changes were then related to seizure outcome, type of surgery, and presurgical disease parameters.

RESULTS

The results demonstrated significant decreases of FC from control group values across the brain after surgery that were not present before surgery, including many contralateral hippocampal connections distal to the surgical site. Postsurgical impairment of contralateral precuneus to ipsilateral occipital connectivity was associated with seizure recurrence. Presurgical impairment of the contralateral precuneus to contralateral temporal lobe connectivity was associated with those who underwent selective amygdalohippocampectomy compared to those who had temporal lobectomy. Finally, changes in thalamic connectivity after surgery were linearly related to duration of epilepsy and frequency of consciousness-impairing seizures prior to surgery.

CONCLUSIONS

The widespread contralateral hippocampal FC changes after surgery may be a reflection of an ongoing epileptogenic progression that has been altered by the surgery, rather than a direct result of the surgery itself. This network evolution may contribute to long-term seizure outcome. Therefore, the combination of presurgical network mapping with the understanding of the dynamic effects of surgery on the networks may ultimately be used to create predictors of the likelihood of long-term seizure recurrence in individual patients after mTLE surgery.

ABBREVIATIONS FC = functional connectivity; fMRI = functional MRI; mTLE = mesial temporal lobe epilepsy.

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Contributor Notes

Correspondence Victoria L. Morgan: Vanderbilt University Institute of Imaging Science, Vanderbilt University, Nashville, TN. victoria.morgan@vanderbilt.edu.

INCLUDE WHEN CITING Published online June 14, 2019; DOI: 10.3171/2019.3.JNS19350.

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

    Besson P, Dinkelacker V, Valabregue R, Thivard L, Leclerc X, Baulac M, : Structural connectivity differences in left and right temporal lobe epilepsy. Neuroimage 100:135144, 2014

    • Search Google Scholar
    • Export Citation
  • 2

    Bettus G, Bartolomei F, Confort-Gouny S, Guedj E, Chauvel P, Cozzone PJ, : Role of resting state functional connectivity MRI in presurgical investigation of mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 81:11471154, 2010

    • Search Google Scholar
    • Export Citation
  • 3

    Bonilha L, Jensen JH, Baker N, Breedlove J, Nesland T, Lin JJ, : The brain connectome as a personalized biomarker of seizure outcomes after temporal lobectomy. Neurology 84:18461853, 2015

    • Search Google Scholar
    • Export Citation
  • 4

    Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, : Frequencies contributing to functional connectivity in the cerebral cortex in “resting-state” data. AJNR Am J Neuroradiol 22:13261333, 2001

    • Search Google Scholar
    • Export Citation
  • 5

    Deleo F, Garbelli R, Milesi G, Gozzo F, Bramerio M, Villani F, : Short- and long-term surgical outcomes of temporal lobe epilepsy associated with hippocampal sclerosis: relationships with neuropathology. Epilepsia 57:306315, 2016

    • Search Google Scholar
    • Export Citation
  • 6

    Elliott CA, Gross DW, Wheatley BM, Beaulieu C, Sankar T: Progressive contralateral hippocampal atrophy following surgery for medically refractory temporal lobe epilepsy. Epilepsy Res 125:6271, 2016

    • Search Google Scholar
    • Export Citation
  • 7

    Engel J, Van Ness PC, Rasmussen TB, Ojemann LM: Outcome with respect to epileptic seizures, in Engel J (ed): Surgical Treatment of the Epilepsies, ed 2. New York: Raven Press, 1993, pp 609621

    • Search Google Scholar
    • Export Citation
  • 8

    Engel J Jr: Mesial temporal lobe epilepsy: what have we learned? Neuroscientist 7:340352, 2001

  • 9

    Engel J Jr: What can we do for people with drug-resistant epilepsy? The 2016 Wartenberg Lecture. Neurology 87:24832489, 2016

  • 10

    Englot DJ, Chang EF: Rates and predictors of seizure freedom in resective epilepsy surgery: an update. Neurosurg Rev 37:389405, 2014

  • 11

    Englot DJ, Konrad PE, Morgan VL: Regional and global connectivity disturbances in focal epilepsy, related neurocognitive sequelae, and potential mechanistic underpinnings. Epilepsia 57:15461557, 2016

    • Search Google Scholar
    • Export Citation
  • 12

    Englot DJ, Mishra AM, Mansuripur PK, Herman P, Hyder F, Blumenfeld H: Remote effects of focal hippocampal seizures on the rat neocortex. J Neurosci 28:90669081, 2008

    • Search Google Scholar
    • Export Citation
  • 13

    Fernandes DA, Yasuda CL, Lopes TM, Enrico G, Alessio A, Tedeschi H, : Long-term postoperative atrophy of contralateral hippocampus and cognitive function in unilateral refractory MTLE with unilateral hippocampal sclerosis. Epilepsy Behav 36:108114, 2014

    • Search Google Scholar
    • Export Citation
  • 14

    Fisher RA: Frequency distribution of the values of the correlation coefficient in samples from an indefinitely large population. Biometrika 10:507521, 1915

    • Search Google Scholar
    • Export Citation
  • 15

    Gleichgerrcht E, Munsell B, Bhatia S, Vandergrift WA III, Rorden C, McDonald C, : Deep learning applied to whole-brain connectome to determine seizure control after epilepsy surgery. Epilepsia 59:16431654, 2018

    • Search Google Scholar
    • Export Citation
  • 16

    Glover GH, Li TQ, Ress D: Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn Reson Med 44:162167, 2000

    • Search Google Scholar
    • Export Citation
  • 17

    Goellner E, Bianchin MM, Burneo JG, Parrent AG, Steven DA: Timing of early and late seizure recurrence after temporal lobe epilepsy surgery. Epilepsia 54:19331941, 2013

    • Search Google Scholar
    • Export Citation
  • 18

    Haneef Z, Lenartowicz A, Yeh HJ, Levin HS, Engel J Jr, Stern JM: Functional connectivity of hippocampal networks in temporal lobe epilepsy. Epilepsia 55:137145, 2014

    • Search Google Scholar
    • Export Citation
  • 19

    He X, Doucet GE, Pustina D, Sperling MR, Sharan AD, Tracy JI: Presurgical thalamic “hubness” predicts surgical outcome in temporal lobe epilepsy. Neurology 88:22852293, 2017

    • Search Google Scholar
    • Export Citation
  • 20

    Huo Y, Plassard AJ, Carass A, Resnick SM, Pham DL, Prince JL, : Consistent cortical reconstruction and multi-atlas brain segmentation. Neuroimage 138:197210, 2016

    • Search Google Scholar
    • Export Citation
  • 21

    Jehi LE, Silveira DC, Bingaman W, Najm I: Temporal lobe epilepsy surgery failures: predictors of seizure recurrence, yield of reevaluation, and outcome following reoperation. J Neurosurg 113:11861194, 2010

    • Search Google Scholar
    • Export Citation
  • 22

    Laxer KD, Trinka E, Hirsch LJ, Cendes F, Langfitt J, Delanty N, : The consequences of refractory epilepsy and its treatment. Epilepsy Behav 37:5970, 2014

    • Search Google Scholar
    • Export Citation
  • 23

    Liu Z, de Zwart JA, Yao B, van Gelderen P, Kuo LW, Duyn JH: Finding thalamic BOLD correlates to posterior alpha EEG. Neuroimage 63:10601069, 2012

    • Search Google Scholar
    • Export Citation
  • 24

    Maccotta L, Lopez MA, Adeyemo B, Ances BM, Day BK, Eisenman LN, : Postoperative seizure freedom does not normalize altered connectivity in temporal lobe epilepsy. Epilepsia 58:18421851, 2017

    • Search Google Scholar
    • Export Citation
  • 25

    Morgan VL, Englot DJ, Rogers BP, Landman BA, Cakir A, Abou-Khalil BW, : Magnetic resonance imaging connectivity for the prediction of seizure outcome in temporal lobe epilepsy. Epilepsia 58:12511260, 2017

    • Search Google Scholar
    • Export Citation
  • 26

    Morgan VL, Rogers BP, Anderson AW, Landman BA, Englot DJ: Divergent network properties that predict early surgical failure versus late recurrence in temporal lobe epilepsy. J Neurosurg [epub ahead of print April 5, 2019. DOI: 10.3171/2019.1.JNS182875]

    • Search Google Scholar
    • Export Citation
  • 27

    Morgan VL, Rogers BP, Sonmezturk HH, Gore JC, Abou-Khalil B: Cross hippocampal influence in mesial temporal lobe epilepsy measured with high temporal resolution functional magnetic resonance imaging. Epilepsia 52:17411749, 2011

    • Search Google Scholar
    • Export Citation
  • 28

    Najm I, Jehi L, Palmini A, Gonzalez-Martinez J, Paglioli E, Bingaman W: Temporal patterns and mechanisms of epilepsy surgery failure. Epilepsia 54:772782, 2013

    • Search Google Scholar
    • Export Citation
  • 29

    Pereira FRS, Alessio A, Sercheli MS, Pedro T, Bilevicius E, Rondina JM, : Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI. BMC Neurosci 11:66, 2010

    • Search Google Scholar
    • Export Citation
  • 30

    Pittau F, Grova C, Moeller F, Dubeau F, Gotman J: Patterns of altered functional connectivity in mesial temporal lobe epilepsy. Epilepsia 53:10131023, 2012

    • Search Google Scholar
    • Export Citation
  • 31

    Rogers BP, Morgan VL, Newton AT, Gore JC: Assessing functional connectivity in the human brain by fMRI. Magn Reson Imaging 25:13471357, 2007

    • Search Google Scholar
    • Export Citation
  • 32

    Wiebe S, Blume WT, Girvin JP, Eliasziw M: A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 345:311318, 2001

    • Search Google Scholar
    • Export Citation
  • 33

    Zou Q, Long X, Zuo X, Yan C, Zhu C, Yang Y, : Functional connectivity between the thalamus and visual cortex under eyes closed and eyes open conditions: a resting-state fMRI study. Hum Brain Mapp 30:30663078, 2009

    • Search Google Scholar
    • Export Citation

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