Facial emotion recognition impairment in chronic temporal lobe epilepsy

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Epilepsia, 50(6):1547–1559, 2009 doi: 10.1111/j.1528-1167.2008.01978.x


Facial emotion recognition impairment in chronic temporal lobe epilepsy *Stefano Meletti, *Francesca Benuzzi, yGaetano Cantalupo, yGuido Rubboli, yCarlo Alberto Tassinari, and *Paolo Nichelli *Department of Neurosciences, Nuovo Ospedale Civile S.Agostino-Estense, University of Modena and Reggio Emilia, Modena, Italy; and yDivision of Neurology, Department of Neurosciences, Bellaria Hospital, University of Bologna, Bologna, Italy

SUMMARY Purpose: To evaluate facial emotion recognition (FER) in a cohort of 176 patients with chronic temporal lobe epilepsy (TLE). Methods: FER was tested by matching facial expressions with the verbal labels for the following basic emotions: happiness, sadness, fear, disgust, and anger. Emotion recognition performances were analyzed in medial (n = 140) and lateral (n = 36) TLE groups. Fifty healthy subjects served as controls. The clinical and neuroradiologic variables potentially affecting the ability to recognize facial expressions were taken into account. Results: The medial TLE (MTLE) group showed impaired FER (86% correct recognition) compared to both the lateral TLE patients (FER = 93.5%) and the controls (FER = 96.4%), with 42% of MTLE patients recording rates of FER that were lower [by at least 2 standard deviations (SDs)] than the control mean. The MTLE group was impaired compared to the healthy controls in

In the past decade, the role and importance of the anteromedial temporal lobe region in decoding the emotions, mental states, and beliefs of others have been demonstrated by a number of lesion and functional imaging studies (Adolphs et al., 1996; Adolphs, 2003). In the field of epilepsy this knowledge has several clinical implications, as well as other, speculative implications. Indeed, temporal lobe epilepsy (TLE), the most common form of focal Accepted October 21, 2008; Early View publication January 21, 2009. Address correspondence to Stefano Meletti, M.D., Ph.D., Department of Neurosciences, University of Modena and Reggio Emilia, Nuovo Ospedale Civile S.Agostino-Estense, Via Giardini, 41100 Modena, Italy. E-mail: [email protected] Wiley Periodicals, Inc. ª 2009 International League Against Epilepsy

the recognition of all basic facial expressions except happiness. The patients with bilateral MTLE were the most severely impaired, followed by the right and then the left MTLE patients. FER was not affected by type of lesion, number of antiepileptic drugs (AEDs), aura semiology, or gender. Conversely, the early onset of seizures/ epilepsy was related to FER deficits. These deficits were already established in young adulthood, with no evidence of progression in older MTLE patients. Conclusion: These results on a large cohort of TLE patients demonstrate that emotion recognition deficits are common in MTLE patients and widespread across negative emotions. We confirm that early onset seizures with right or bilateral medial temporal dysfunction lead to severe deficits in recognizing facial expressions of emotions. KEY WORDS: Temporal lobe epilepsy, Neuropsychology, Emotion recognition, Facial expression, Medial temporal sclerosis.

epilepsy, is frequently characterized by lesions or gliosis/ atrophy (hippocampal sclerosis) involving the medial temporal lobe region (Williamson et al., 1993; Wieser, 2004). Moreover, anteromedial temporal lobe resection is the ‘‘standard’’ treatment for drug-resistant medial TLE (Wiebe et al., 2001; Tellez-Zenteno et al., 2007). Consequently, the investigation of emotional and social competence in patients with TLE has been the focus of different studies (Meletti et al., 2003; Reynders et al., 2005; Yamada et al., 2005; Schacher et al., 2006; Shaw et al., 2007), which have extended the scope of neuropsychological evaluation in TLE beyond the traditional evaluation of memory, language, and executive functions (Hermann et al., 1997, 2006; Helmstaedter et al., 2003). The first facial emotion recognition (FER) studies investigated cohorts of TLE patients after surgery and demonstrated


1548 S. Meletti et al. that subjects can show impaired FER after unilateral temporal lobectomy, especially after nondominant rightside resections (Anderson et al., 2000; Adolphs et al., 2001). Subsequently, we demonstrated that chronic drugresistant epilepsy involving the medial temporal region is associated with deficits in emotion recognition even before surgery (Meletti et al., 2003). An important question concerning the recognition of facial expressions is whether there exists a critical period of life for establishing the neural network involved in this ability. Our previous results suggested that early insults to the right medial temporal structures could play a crucial role in causing FER impairments (Meletti et al., 2003; Benuzzi et al., 2004). This pattern of deficit has been observed in studies addressing the impact of early seizures on ‘‘theory of mind’’ tasks (Shaw et al., 2004), emotional memory (Shaw et al., 2005), and recently in a study analyzing FER (McClelland et al., 2006). Other studies, however, have not confirmed these correlations between emotion recognition deficits and epilepsy-related variables (Brierley et al., 2004; Glogau et al., 2004; Fowler et al., 2006). Differences across studies could be attributable to various causes: small numbers of patients investigated, different tasks used, and different grouping/selection criteria. In this article we present the results of a large crosssectional cohort study investigating FER in 176 patients with TLE. Emotion recognition performances were analyzed in medial and lateral TLE groups. The clinical and neuroradiologic variables potentially affecting the ability to recognize facial expressions of basic emotions were taken into account. In particular, the purpose is to evaluate if epilepsy and seizure-related variables, such as the age at epilepsy onset, epilepsy duration, the type of aura, or the drugs used could affect emotion recognition in a large cohort of patients with chronic TLE.

Materials and Methods Patient and control groups Patients were recruited and evaluated over a 5-year period, from January 2003 to December 2007. Subjects reported in previous publications were not included in the study. On the basis of clinical history and neurophysiolog-

ic and magnetic resonance imaging (MRI) findings, 176 patients with symptomatic TLE were selected for the study. The subjects were referred from three epilepsy centers (Division of Neurology, Dept of Neurosciences– Bellaria Hospital, University of Bologna; Dept of Neurosciences, Nuovo Ospedale Civile S.Agostino-Estense, University of Modena and Reggio Emilia; and ‘‘C. Munari’’ Epilepsy and Parkinson’s Disease Surgery Centre, Niguarda Hospital, Milan) and were evaluated for possible epilepsy surgery. In all the patients, noninvasive neurophysiologic evaluation was based on interictal electroencephalography (EEG) recordings and prolonged video-EEG monitoring to document the patient’s habitual seizures. Clinical and EEG features of the seizures were analyzed to obtain an objective evaluation of ictal semiology and to establish the cerebral structures involved in the epileptic activity. MRI (1.5 or 3.0 Tesla) was performed in all patients to investigate the temporal lobe structures in detail. The presence of medial temporal sclerosis (MTS) was evaluated qualitatively by visual inspection of the MR images: both atrophy (on T1-weighted sequences) and increased medial temporal signal intensity [on T2-weighted and fluid-attenuated inversion recovery (FLAIR) sequences] were necessary to diagnose MTS. The patients were divided into two groups on the basis of anatomo-electroclinical correlations (see Tables 1 and 2): (1) Medial temporal lobe epilepsy patients (MTLE group, n = 140) with evidence of MTS or other medial temporal lobe lesions on MRI (involving the amygdala and/or hippocampus). (2) Lateral temporal lobe epilepsy patients (LTLE group, n = 36) with MRI evidence of temporal lobe lesions located in the lateral temporal cortex. We took care to enroll in the study only patients with clear-cut MRI findings. Patients with MRI imaging not clearly diagnostic or with cryptogenic epilepsy were not included. Patients with double pathology on MRI such as lateral or temporobasal lesions plus MTS were not enrolled in the study. Detailed lesions descriptions are provided in Table 2. Fifty right-handed (Oldfield, 1971) healthy volunteers with no history of neurologic or psychiatric illness participated as healthy controls (CTRL).

Table 1. Demographic features of controls and patient groups



Age (years) Mean (±SD)

Sex (m/f)


Years of educationb Mean (±SD)

50 36 140

34.9 (±9.1) 37.1 (±11.6) 38.6 (±9.9)

20/30 16/20 63/77

50 36 131

16.1 (±2.4) 12.3 (±3.4) 11.6 (±3.5)

CTRL, healthy controls; LTLE, lateral temporal lobe epilepsy group; MTLE, medial temporal lobe epilepsy group. a Evaluated using the Edinburgh Inventory (Oldfield, 1971). b The CTRL group had a higher number of years of education compared to both patient groups (p < 0.01). Epilepsia, 50(6):1547–1559, 2009 doi: 10.1111/j.1528-1167.2008.01978.x

1549 Facial Expression Recognition and TLE Table 2. Clinical features of patient groups Febrile convulsions, n (%) Age at first seizure (years), Mean (±SD) Age at epilepsy onset (years), Mean (±SD) Years with epilepsy, Mean (±SD) Hemisphere of seizure onset, Right/left/bilateral MRI findings, n (%) Medial temporal sclerosis Focal cortical dysplasia DNET/ganglioglioma Cavernoma Posttraumatic gliosis Low grade tumors Arteriovenous malformation Postencephalitic gliosis Postsurgical scar Perinatal ischemic lesion

LTLE (n = 36)

MTLE (n = 140)


6 (17) 15.5 (±11.1) 18.5 (±11.2) 18.6 (±12.9) 20/16

60 (43) 9.6 (±10.9) 13.3 (±10.3) 25.3 (±11.7) 68/59/13

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