Advertisement
Research Article| Volume 142, 109191, May 2023

Download started.

Ok

Revisiting emotion recognition in different types of temporal lobe epilepsy: The influence of facial expression intensity

  • C. Nineuil
    Affiliations
    Univ. Lille, ULR 4072 - PSITEC - Psychologie : Interactions Temps Émotions Cognition, F-59000 Lille, France
    Search for articles by this author
  • M. Houot
    Affiliations
    Centre of Excellence of Neurodegenerative Disease (CoEN), AP-HP, Pitié-Salpêtrière Hospital, Paris, France

    Institute of Memory and Alzheimer's Disease (IM2A), Department of Neurology, AP-HP, Pitié-Salpêtrière Hospital, Paris, France

    Clinical Investigation Centre, Institut du Cerveau et de la Moelle épinière (ICM), Pitié-Salpêtrière Hospital, Paris, France
    Search for articles by this author
  • D. Dellacherie
    Affiliations
    Univ. Lille, ULR 4072 - PSITEC - Psychologie : Interactions Temps Émotions Cognition, F-59000 Lille, France

    CHU Lille, Department of Pediatric Neurology, F-59000 Lille, France
    Search for articles by this author
  • M. Méré
    Affiliations
    Epilepsy Unit, AP-HP, Pitié-Salpêtrière Hospital, Paris, France
    Search for articles by this author
  • M. Denos
    Affiliations
    Rehabilitation Unit, AP-HP, Pitié-Salpêtrière Hospital, Paris, France
    Search for articles by this author
  • S. Dupont
    Affiliations
    Epilepsy Unit, AP-HP, Pitié-Salpêtrière Hospital, Paris, France

    Centre de Recherche de l’Institut du Cerveau Et de La Moelle Épinière (ICM), UMPC-UMR 7225 CNRS-UMRS 975 Inserm, Paris, France
    Search for articles by this author
  • S. Samson
    Correspondence
    Corresponding author at: Université de Lille, Domaine Universitaire du Pont de Bois, Laboratoire PSITEC (ULR 4072), Rue du Barreau BP 60149 59653 Villeneuve d'Ascq Cedex, France.
    Affiliations
    Univ. Lille, ULR 4072 - PSITEC - Psychologie : Interactions Temps Émotions Cognition, F-59000 Lille, France

    Epilepsy Unit, AP-HP, Pitié-Salpêtrière Hospital, Paris, France

    Centre de Recherche de l’Institut du Cerveau Et de La Moelle Épinière (ICM), UMPC-UMR 7225 CNRS-UMRS 975 Inserm, Paris, France
    Search for articles by this author

      Highlights

      • Emotional facial recognition is not globally impaired in TLE.
      • TLE patients show deficits in recognizing facial expressions of fear and disgust.
      • Localization of epilepsy focus plays a role in recognizing specific expressions.
      • Sensitivity to emotional intensity varies with epilepsy localization and emotion.

      Abstract

      Temporal lobe epilepsy (TLE) can induce various difficulties in recognizing emotional facial expressions (EFE), particularly for negative valence emotions. However, these difficulties have not been systematically examined according to the localization of the epileptic focus. For this purpose, we used a forced-choice recognition task in which faces expressing fear, sadness, anger, disgust, surprise, or happiness were presented in different intensity levels from moderate to high intensity. The first objective of our study was to evaluate the impact of emotional intensity on the recognition of different categories of EFE in TLE patients compared to control participants. The second objective was to assess the effect of localization of epileptic focus on the recognition of EFE in patients with medial temporal lobe epilepsy (MTLE) associated or not with hippocampal sclerosis (HS), or lateral temporal lobe epilepsy (LTLE). The results showed that the 272 TLE patients and the 68 control participants were not differently affected by the intensity of EFE. However, we obtained group differences within the clinical population when we took into account the localization of the temporal lobe epileptic focus. As predicted, TLE patients were impaired in recognizing fear and disgust relative to controls. Moreover, the scores of these patients varied according to the localization of the epileptic focus, but not according to the cerebral lateralization of TLE. The facial expression of fear was less well recognized by MTLE patients, with or without HS, and the expression of disgust was less well recognized by LTLE as well as MTLE without HS patients. Moreover, emotional intensity modulated differently the recognition of disgust and surprise of the three patient groups underlying the relevance of using moderate emotional intensity to distinguish the effect of epileptic focus localization. These findings should be taken into account for interpreting the emotional behaviors and deserve to be further investigated before considering TLE surgical treatment or social cognition interventions in TLE patients.

      Keywords

      Abbreviations:

      TLE (Temporal lobe epilepsy), EFE (Emotional facial expressions), MTLE (Medial temporal lobe epilepsy), HS (Hippocampal sclerosis), LTLE (Lateral temporal lobe epilepsy), ASMs (Anti-seizure medications)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Epilepsy & Behavior
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Adolphs R.
        Neural systems for recognizing emotion.
        Curr Opin Neurobiol. 2002; 12: 169-177https://doi.org/10.1016/S0959-4388(02)00301-X
        • Adolphs R.
        Cognitive neuroscience of human social behaviour.
        Nat Rev Neurosci. 2003; 4: 165-178https://doi.org/10.1038/nrn1056
        • Adolphs R.
        What does the amygdala contribute to social cognition?.
        Ann N Y Acad Sci. 2010; 1191: 42-61https://doi.org/10.1111/j.1749-6632.2010.05445.x
        • Adolphs R.
        • Tranel D.
        • Damasio H.
        Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala.
        Nature. 1994; 372: 4
        • Adolphs R.
        • Tranel D.
        • Damasio H.
        • Damasio A.R.
        Fear and the human amygdala.
        J Neurosci. 1995; 15: 5879-5891
        • Adolphs R.
        • Tranel D.
        • Hamann S.B.
        • Young A.W.
        • Calder A.J.
        • Phelps E.A.
        • et al.
        Recognition of facial emotion in nine individuals with bilateral amygdala damage.
        Neuropsychologia. 1999; 37: 1111-1117https://doi.org/10.1016/S0028-3932(99)00039-1
        • Allone C.
        • Buono V.L.
        • Corallo F.
        • Pisani L.R.
        • Pollicino P.
        • Bramanti P.
        • et al.
        Neuroimaging and cognitive functions in temporal lobe epilepsy: A review of the literature.
        J Neurol Sci. 2017; 381: 7-15
        • Amlerova J.
        • Cavanna A.E.
        • Bradac O.
        • Javurkova A.
        • Raudenska J.
        • Marusic P.
        Emotion recognition and social cognition in temporal lobe epilepsy and the effect of epilepsy surgery.
        Epilepsy Behav. 2014; 36: 86-89https://doi.org/10.1016/j.yebeh.2014.05.001
        • Anderson A.K.
        • Phelps E.A.
        Expression Without Recognition: Contributions of the Human Amygdala to Emotional Communication.
        Psychol Sci. 2000; 11: 106-111https://doi.org/10.1111/1467-9280.00224
        • Arioli M.
        • Crespi C.
        • Canessa N.
        Social Cognition through the Lens of Cognitive and Clinical Neuroscience.
        Biomed Res Int. 2018; 2018: e4283427https://doi.org/10.1155/2018/4283427
      1. Benton AL, Hamsher K deS, Varney NR, Spreen O. Contributions to neuropsychological assessment: a clinical manual. 2nd ed. Oxford University Press; 1983.

        • Blümcke I.
        • Thom M.
        • Aronica E.
        • Armstrong D.D.
        • Bartolomei F.
        • Bernasconi A.
        • et al.
        International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: A Task Force report from the ILAE Commission on Diagnostic Methods.
        Epilepsia. 2013; 54: 1315-1329https://doi.org/10.1111/epi.12220
        • Bonora A.
        • Benuzzi F.
        • Monti G.
        • Mirandola L.
        • Pugnaghi M.
        • Nichelli P.
        • et al.
        Recognition of emotions from faces and voices in medial temporal lobe epilepsy.
        Epilepsy Behav. 2011; 20: 648-654https://doi.org/10.1016/j.yebeh.2011.01.027
        • Bora E.
        • Meletti S.
        Social cognition in temporal lobe epilepsy: A systematic review and meta-analysis.
        Epilepsy Behav. 2016; 60: 50-57https://doi.org/10.1016/j.yebeh.2016.04.024
        • Broicher S.D.
        • Kuchukhidze G.
        • Grunwald T.
        • Krämer G.
        • Kurthen M.
        • Jokeit H.
        “Tell me how do I feel” – Emotion recognition and theory of mind in symptomatic mesial temporal lobe epilepsy.
        Neuropsychologia. 2012; 50: 118-128https://doi.org/10.1016/j.neuropsychologia.2011.11.005
        • Bruyer R.
        • Granato P.
        Categorical effects in the perception of facial expressions; MARIE - A simple and discriminating clinical tool.
        Rev Eur Psychol Appl. 1999; 49: 3
        • Calder A.J.
        • Keane J.
        • Manes F.
        • Antoun N.
        • Young A.W.
        Impaired recognition and experience of disgust following brain injury.
        Nat Neurosci. 2000; 3: 1077-1078https://doi.org/10.1038/80586
      2. Calder AJ, Young AW, Rowland D, Perrett DI, Hodges JR, EtcoΠNL. Facial Emotion Recognition after Bilateral Amygdala Damage: Differentially Severe Impairment of Fear 1996;47.

        • Calvo M.G.
        • Lundqvist D.
        Facial expressions of emotion (KDEF): Identification under different display-duration conditions.
        Behav Res Methods. 2008; 40: 109-115https://doi.org/10.3758/BRM.40.1.109
        • Cheng C.-M.
        • Chen H.-C.
        • Chan Y.-C.
        • Su Y.-C.
        • Tseng C.-C.
        Taiwan corpora of Chinese emotions and relevant psychophysiological data—Normative data for Chinese jokes.
        Chinese J Psychol. 2013; 55: 555-569
        • Dellacherie D.
        • Hasboun D.
        • Baulac M.
        • Belin P.
        • Samson S.
        Impaired recognition of fear in voices and reduced anxiety after unilateral temporal lobe resection.
        Neuropsychologia. 2011; 49: 618-629https://doi.org/10.1016/j.neuropsychologia.2010.11.008
        • Edwards M.
        • Stewart E.
        • Palermo R.
        • Lah S.
        Facial emotion perception in patients with epilepsy: A systematic review with meta-analysis.
        Neurosci Biobehav Rev. 2017; 83: 212-225https://doi.org/10.1016/j.neubiorev.2017.10.013
        • Ekman P.
        An argument for basic emotions.
        Cogn Emot. 1992; 6: 169-200
        • Ekman P.
        • Friesen W.V.
        Measuring facial movement.
        Environ Psychol Nonverbal Behav. 1976; 1: 56-75
        • Ekman P.
        • Friesen W.V.
        Unmasking the Face: A Guide to Recognizing Emotions from Facial Clues.
        ISHK. 2003;
        • Feldman Barrett L.
        • Russell J.A.
        Independence and bipolarity in the structure of current affect.
        J Pers Soc Psychol. 1998; 74: 967-984https://doi.org/10.1037/0022-3514.74.4.967
        • Fusar-Poli P.
        • Placentino A.
        • Carletti F.
        • Landi P.
        • Allen P.
        • Surguladze S.
        • et al.
        Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies.
        J Psychiatry Neurosci: JPN. 2009; 34: 418-432
      3. Giovagnoli AR, Parente A, Ciuffini R, Tallarita GM, Turner K, Maialetti A, et al. & the Study Group on Cognitive Neurology, Neuropsychology – Adult Section of the Italian League AgainstEpilepsy. Diversified social cognition in temporal lobe epilepsy. Acta Neurol Scandinavica 2021;143(4):396–406. https://doi.org/10.1111/ane.13386.

        • Giovagnoli A.R.
        • Parente A.
        • Villani F.
        • Franceschetti S.
        • Spreafico R.
        Theory of mind and epilepsy: What clinical implications?.
        Epilepsia. 2013; 54: 1639-1646https://doi.org/10.1111/epi.12255
        • Gomez-Ibañez A.
        • Urrestarazu E.
        • Viteri C.
        Recognition of facial emotions and identity in patients with mesial temporal lobe and idiopathic generalized epilepsy: An eye-tracking study.
        Seizure. 2014; 23: 892-898https://doi.org/10.1016/j.seizure.2014.08.012
        • Gosselin N.
        • Peretz I.
        • Hasboun D.
        • Baulac M.
        • Samson S.
        Impaired recognition of musical emotions and facial expressions following anteromedial temporal lobe excision.
        Cortex. 2011; 47: 1116-1125https://doi.org/10.1016/j.cortex.2011.05.012
        • Granato P.
        • Bruyer R.
        Measurement of the perception of facially expressed emotions by a computerized device: Method of analysis and research for the integration of emotions (MARIE).
        Eur Psychiatry. 2002; 17: 339-348https://doi.org/10.1016/S0924-9338(02)00684-3
        • Habel U.
        • Windischberger C.
        • Derntl B.
        • Robinson S.
        • Kryspin-Exner I.
        • Gur R.C.
        • et al.
        Amygdala activation and facial expressions: Explicit emotion discrimination versus implicit emotion processing.
        Neuropsychologia. 2007; 45: 2369-2377https://doi.org/10.1016/j.neuropsychologia.2007.01.023
        • Hennion S.
        • Szurhaj W.
        • Duhamel A.
        • Lopes R.
        • Tyvaert L.
        • Derambure P.
        • et al.
        Characterization and prediction of the recognition of emotional faces and emotional bursts in temporal lobe epilepsy.
        J Clin Exp Neuropsychol. 2015; 37: 931-945https://doi.org/10.1080/13803395.2015.1068280
        • Hermann B.
        • Seidenberg M.
        • Jones J.
        The neurobehavioural comorbidities of epilepsy: Can a natural history be developed?.
        Lancet Neurol. 2008; 7: 151-160https://doi.org/10.1016/S1474-4422(08)70018-8
        • Hess U.
        • Blairy S.
        • Kleck R.E.
        The Intensity of Emotional Facial Expressions and Decoding Accuracy.
        J Nonverbal Behav. 1997; 21: 241-257https://doi.org/10.1023/A:1024952730333
        • Hlobil U.
        • Rathore C.
        • Alexander A.
        • Sarma S.
        • Radhakrishnan K.
        Impaired facial emotion recognition in patients with mesial temporal lobe epilepsy associated with hippocampal sclerosis (MTLE-HS): Side and age at onset matters.
        Epilepsy Res. 2008; 80: 150-157https://doi.org/10.1016/j.eplepsyres.2008.03.018
        • Kotwas I.
        • McGonigal A.
        • Bastien-Toniazzo M.
        • Bartolomei F.
        • Micoulaud-Franchi J.-A.
        Stress regulation in drug-resistant epilepsy.
        Epilepsy Behav. 2017; 71: 39-50https://doi.org/10.1016/j.yebeh.2017.01.025
        • Krolak-Salmon P.
        • Hénaff M.-A.
        • Isnard J.
        • Tallon-Baudry C.
        • Guénot M.
        • Vighetto A.
        • et al.
        An attention modulated response to disgust in human ventral anterior insula.
        Ann Neurol. 2003; 53: 446-453https://doi.org/10.1002/ana.10502
        • Lin Y.-H.
        • Hsin Y.-L.
        • Li R.-H.
        • Liu C.-K.
        • Wang R.-Y.
        • Wang W.-H.
        The effect of facial expression intensity on emotion recognition and psychosocial performance in patients with frontal or temporal lobe epilepsy.
        Epilepsy Behav. 2022; 126108462https://doi.org/10.1016/j.yebeh.2021.108462
        • Meletti S.
        • Benuzzi F.
        • Cantalupo G.
        • Rubboli G.
        • Tassinari C.A.
        • Nichelli P.
        Facial emotion recognition impairment in chronic temporal lobe epilepsy.
        Epilepsia. 2009; 50: 1547-1559https://doi.org/10.1111/j.1528-1167.2008.01978.x
        • Meletti S.
        • Benuzzi F.
        • Nichelli P.
        • Tassinari C.A.
        Damage to the Right Hippocampal-Amygdala Formation during Early Infancy and Recognition of Fearful Faces: Neuropsychological and fMRI Evidence in Subjects with Temporal Lobe Epilepsy.
        Ann N Y Acad Sci. 2003; 1000: 385-388https://doi.org/10.1196/annals.1280.036
        • Meletti S.
        • Benuzzi F.
        • Rubboli G.
        • Cantalupo G.
        • Stanzani Maserati M.
        • Nichelli P.
        • et al.
        Impaired facial emotion recognition in early-onset right mesial temporal lobe epilepsy.
        Neurology. 2003; 60: 426-431https://doi.org/10.1212/WNL.60.3.426
        • Meletti S.
        • Cantalupo G.
        • Santoro F.
        • Benuzzi F.
        • Marliani A.F.
        • Tassinari C.A.
        • et al.
        Temporal lobe epilepsy and emotion recognition without amygdala: A case study of Urbach-Wiethe disease and review of the literature.
        Epileptic Disord. 2014; 16: 518-527https://doi.org/10.1684/epd.2014.0696
        • Meletti S.
        • Picardi A.
        • De Risi M.
        • Monti G.
        • Esposito V.
        • Grammaldo L.G.
        • et al.
        The affective value of faces in patients achieving long-term seizure freedom after temporal lobectomy.
        Epilepsy Behav. 2014; 36: 97-101https://doi.org/10.1016/j.yebeh.2014.05.002
        • Monti G.
        • Meletti S.
        Emotion recognition in temporal lobe epilepsy: A systematic review.
        Neurosci Biobehav Rev. 2015; 55: 280-293https://doi.org/10.1016/j.neubiorev.2015.05.009
        • Orgeta V.
        • Phillips L.H.
        Effects of age and emotional intensity on the recognition of facial emotion.
        Exp Aging Res. 2008; 34: 63-79https://doi.org/10.1080/03610730701762047
        • Ortony A.
        • Turner T.J.
        What’s basic about basic emotions?.
        Psychol Rev. 1990; 97: 315
        • Palermo R.
        • Coltheart M.
        Photographs of facial expression: Accuracy, response times, and ratings of intensity.
        Behav Res Methods Instrum Comput. 2004; 36: 634-638https://doi.org/10.3758/BF03206544
        • Phillips M.L.
        • Young A.W.
        • Senior C.
        • Brammer M.
        • Andrew C.
        • Calder A.J.
        • et al.
        A specific neural substrate for perceiving facial expressions of disgust.
        Nature. 1997; 389: 495-498https://doi.org/10.1038/39051
        • Reynders H.J.
        • Broks P.
        • Dickson J.M.
        • Lee C.E.
        • Turpin G.
        Investigation of social and emotion information processing in temporal lobe epilepsy with ictal fear.
        Epilepsy Behav. 2005; 7: 419-429https://doi.org/10.1016/j.yebeh.2005.07.013
        • Sedda A.
        • Rivolta D.
        • Scarpa P.
        • Burt M.
        • Frigerio E.
        • Zanardi G.
        • et al.
        Ambiguous emotion recognition in temporal lobe epilepsy: The role of expression intensity.
        Cogn Affect Behav Neurosci. 2013; 13: 452-463https://doi.org/10.3758/s13415-013-0153-y
        • Steiger B.K.
        • Jokeit H.
        Why epilepsy challenges social life.
        Seizure. 2017; 44: 194-198https://doi.org/10.1016/j.seizure.2016.09.008
        • Steiger B.K.
        • Muller A.M.
        • Spirig E.
        • Toller G.
        • Jokeit H.
        Mesial temporal lobe epilepsy diminishes functional connectivity during emotion perception.
        Epilepsy Res. 2017; 134: 33-40https://doi.org/10.1016/j.eplepsyres.2017.05.004
        • Stewart E.
        • Lah S.
        • Smith M.L.
        Patterns of impaired social cognition in children and adolescents with epilepsy: The borders between different epilepsy phenotypes.
        Epilepsy Behav. 2019; 100106146https://doi.org/10.1016/j.yebeh.2019.01.031
        • Tanaka A.
        • Akamatsu N.
        • Yamano M.
        • Nakagawa M.
        • Kawamura M.
        • Tsuji S.
        A more realistic approach, using dynamic stimuli, to test facial emotion recognition impairment in temporal lobe epilepsy.
        Epilepsy Behav. 2013; 28: 12-16https://doi.org/10.1016/j.yebeh.2013.03.022
        • Vallat-Azouvi C.
        • Azouvi P.
        • Le-Bornec G.
        • Brunet-Gouet E.
        Treatment of social cognition impairments in patients with traumatic brain injury: A critical review.
        Brain Inj. 2019; 33: 87-93https://doi.org/10.1080/02699052.2018.1531309
        • Volfart A.
        • Jonas J.
        • Maillard L.
        • Busigny T.
        • Rossion B.
        • Brissart H.
        Typical visual unfamiliar face individuation in left and right mesial temporal epilepsy.
        Neuropsychologia. 2020; 147107583https://doi.org/10.1016/j.neuropsychologia.2020.107583
        • Wang S.
        • Tudusciuc O.
        • Mamelak A.N.
        • Ross I.B.
        • Adolphs R.
        • Rutishauser U.
        Neurons in the human amygdala selective for perceived emotion.
        Proc Natl Acad Sci. 2014; 111https://doi.org/10.1073/pnas.1323342111
        • Wells L.J.
        • Gillespie S.M.
        • Rotshtein P.
        Identification of Emotional Facial Expressions: Effects of Expression, Intensity, and Sex on Eye Gaze.
        PLoS One. 2016; 11: e0168307https://doi.org/10.1371/journal.pone.0168307
        • Wieser H.G.
        ILAE Commission Report. Mesial temporal lobe epilepsy with hippocampal sclerosis.
        Epilepsia. 2004; 45: 695-714https://doi.org/10.1111/j.0013-9580.2004.09004.x
        • Xu P.
        • Peng S.
        • Luo Y.
        • Gong G.
        Facial expression recognition: A meta-analytic review of theoretical models and neuroimaging evidence.
        Neurosci Biobehav Rev. 2021; 127: 820-836https://doi.org/10.1016/j.neubiorev.2021.05.023