Impaired facial emotion recognition
in early-onset right mesial temporal
lobe epilepsy
S. Meletti, MD; F. Benuzzi, PhD; G. Rubboli, MD; G. Cantalupo, MD; M. Stanzani Maserati, MD;
P. Nichelli, MD; and C.A. Tassinari, MD
Abstract—Background: Anteromedial temporal lobe regions, particularly the amygdala, participate in the recognition of
emotions from facial expressions. The authors studied the ability of facial emotion recognition (ER) in subjects with
symptomatic epilepsy, evaluating whether mesial temporal lobe damage is related to an impairment in the recognition of
specific emotions and whether the onset of seizures in a critical period of life could prevent the development of ER.
Methods: Groups included patients with temporal lobe epilepsy (TLE) with MRI evidence of mesial temporal sclerosis
(MTS) (n = 33); patients with TLE with MRI evidence of temporal lobe lesions other than MTS (n = 30); and patients with
extratemporal epilepsy (n = 33). Healthy volunteers (n = 50) served as controls. ER was tested by matching a facial
expression with the name of one of the following basic emotions: happiness, sadness, fear, disgust, and anger. A
face-matching task was used to control visuoperceptual abilities with face stimuli. Results: No subject showed deficits in
the face-matching task. ER was impaired in patients with right MTS, especially for fearful faces. Patients presenting left
MTS, right or left temporal lobe lesions other than MTS, or extratemporal seizure foci showed ER performances similar to
controls. In all subjects with right TLE, the degree of emotion recognition impairment was related to age at first seizure
(febrile or afebrile) and age at epilepsy onset. Conclusions: Early-onset right-sided mesial temporal lobe epilepsy is the key
substrate determining a severe deficit in recognizing emotional facial expressions, especially fear.
NEUROLOGY 2003;60:426 –431
The amygdala plays a crucial role in the elaboration
and expression of the appropriate autonomic and be-
havioral responses to emotional relevant stimuli.
1-3
In humans, functional imaging studies demonstrated
that the amygdala participates in facial expression
processing.
4-6
Accordingly, lesion studies showed the
importance of the amygdala and related structures of
the anterior and medial temporal lobes in the recog-
nition of emotions from visual stimuli.
7-11
There is
evidence that subjects with bilateral amygdala dam-
age typically fail to recognize facial expressions, es-
pecially fear.
7-11
In patients with temporal lobe epilepsy (TLE), the
amygdala complex is one component of the temporal
lobe that is often damaged, together with the hip-
pocampus.
12,13
The collective term mesial temporal
sclerosis (MTS) was introduced to describe neuronal
loss and gliosis encompassing the hippocampus, the
entorhinal cortex, and the amygdala complex.
13-16
Isolated amygdala damage also occurs in about 10%
of patients with TLE.
17,18
Baseline neuropsychological evaluation of patients
with drug-resistant TLE is usually confined to tasks
assessing language, memory, visuospatial, and exec-
utive abilities. Studies investigating emotion recog-
nition (ER) in patients after unilateral temporal
lobectomy for epilepsy treatment provided somewhat
conflicting findings.
19-22
More importantly, these
studies cannot establish whether impaired recogni-
tion of emotions from facial expressions is related to
the effects of the lobectomy per se or to the effects of
the pre-existing epileptogenic lesion. Moreover, TLE
is not a uniform entity and etiologic factors like the
type and extension of the epileptogenic lesion and
other clinical variables, particularly age at seizure
onset, could play a major role in determining the
quality and entity of the ER deficit. To establish
whether the ER impairment is specific to subjects
with TLE, patients with symptomatic epilepsies re-
lated to extratemporal seizure foci need to be tested.
This study investigated the ability of ER from fa-
cial expressions in subjects with TLE with MRI evi-
dence of MTS. Their performance was then compared
with that of epileptic subjects with other temporal or
extratemporal lesions to determine whether there is a
critical period of life for establishing the neural cir-
cuitry involved in ER.
Materials and methods. Patients selection. Based on neuro-
physiologic and MRI findings 96 patients were selected for the
study. Patients were evaluated between January 1998 and Febru-
From the Division of Neurology (Drs. Meletti, Rubboli, Cantalupo, Stanzani Maserati, and Tassinari), Department of Neurosciences, Bellaria Hospital,
University of Bologna; and Department of Neurosciences (Drs. Benuzzi and Nichelli), University of Modena and Reggio Emilia, Modena, Italy.
Supported by a grant from the Ministero Italiano dell’Università e della Ricerca scientifica (MIUR, ex-40%).
Received July 26, 2002. Accepted in final form October 3, 2002.
Address correspondence and reprint requests to Dr. Stefano Meletti, Division of Neurology, Bellaria Hospital, University of Bologna, Via Altura n° 3, Bologna
40139, Italy; e-mail: stefano.meletti@neuro.unibo.it
426 Copyright © 2003 by AAN Enterprises, Inc.