Seizure: European Journal of Epilepsy 93 (2021) 63–74

Contents lists available at ScienceDirect

Seizure: European Journal of Epilepsy

journal homepage: www.elsevier.com/locate/seizure

Review

Emotion recognition and theory of mind after temporal lobe epilepsy

surgery: A systematic review
Bernadett Mikula a, *, Anita Lencsés a, Csaba Borbély b, Gyula Demeter a, c
a
Department of Cognitive Science, Budapest University of Technology and Economics, Budapest, Hungary
b
National Institute of Mental Health, Neurology and Neurosurgery, Budapest, Hungary
c
Rehabilitation Department of Brain Injuries, National Institute of Medical Rehabilitation, Budapest, Hungary

A R T I C L E I N F O A B S T R A C T

Keywords: In order to navigate in our complex social world successfully, it is crucial to maintain and practice cognitive skills
Temporal lobe epilepsy that are dedicated to adaptive social functioning. Emerging evidence suggests that besides deficits in declarative
Surgery memory, executive functions, and language, impairments in social cognition (SC, e.g., emotion recognition,
Social cognition
theory of mind) are also present in temporal lobe epilepsy (TLE). The organic and psycho-social consequences of
Theory of mind
epilepsy surgery might have additional implications regarding this deficit. Here we qualitatively synthesize
Emotion recognition
longitudinal and cross-sectional findings on SC after TLE surgery. A literature search using PubMed and Scopus
identified 275 potential articles. Studies were eligible if they (1) included patients with a diagnosis of TLE, (2)
included a healthy comparison group, (3) reported original research, (4) were published in peer-reviewed
journals and in English language, (5) reported the intervention of epilepsy surgery. Articles that (1) were case
studies, (2) did not focus on SC abilities, (3) used interviews or self-report questionnaires to examine SC functions
were excluded. A total of 16 original studies assessing emotion recognition (ER) and/or theory of mind (ToM)
matched our criteria. The literature suggests that neither ER nor ToM abilities change after surgery: post-surgery
patients show similar impairment patterns to pre-surgery patients. Nevertheless, individual improvement or
decline could be masked by group comparisons and results should be considered in light of methodological
heterogeneity among studies.

1. Introduction
A substantial part of human cognition is inherently social. In order to
navigate in our complex social world successfully, it is crucial to
maintain and practice cognitive skills that are dedicated to adaptive
social functioning. Impairments in this domain may impede indepen­
dent living since the integrity of these skills contributes to the accom­
plishment of both interpersonal and occupational demands. Considering
the neurocognitive and psycho-social burden affecting people with ep­
ilepsy, this population is more at risk of encountering such problems [1].
The most common form of drug-resistant focal epilepsies in adulthood is
temporal lobe epilepsy (TLE), which is recognized as a complex network
or system disorder affecting distributed brain regions interconnected by
functional and structural networks [2]. In clinical practice, it is divided
into medial and lateral TLE, however, according to the latest classifi­
cation of the International League Against Epilepsy (ILAE), only medi­
otemporal lobe epilepsy (mTLE) with hippocampal sclerosis constitutes
a distinct epilepsy syndrome [3]. People living with TLE face the chal­
lenges of both seizures and cognitive disturbances associated with the
disorder. Traditionally, TLE has been described to be accompanied by
deficits in episodic memory [4,5], executive functions [6], language [7],
and processing speed [8] in various degrees. Recently, it has been
highlighted that the heterogeneity of TLE manifests in distinct cognitive
phenotypes which can be identified with neuropsychological criteria as
well as data-driven methods (e.g. cluster-analysis; [9]). In the past
decade, emerging evidence has been accumulated to suggest that be­
sides deficits in memory, language, and executive functions,
social-cognitive impairments are also present in TLE [10]. This finding

Abbreviations: AEDs, antiepileptic drugs; ATL, anterior temporal lobectomy; EBA, extrastriate body area; ER, emotion recognition; FPR, Faux pas recognition test;
mTLE, mediotemporal lobe epilepsy; MTS, mediotemporal sclerosis; pSTS, posterior superior temporal sulcus; SAH, selective amygdalo-hippocampectomy; SC, social
cognition; TLE, temporal lobe epilepsy; ToM, theory of mind.
* Corresponding author at: Egry József St. 1, 1111 Budapest, Hungary.
E-mail address: mikula.bernadett@ttk.bme.hu (B. Mikula).

https://doi.org/10.1016/j.seizure.2021.10.005
Received 30 May 2021; Received in revised form 13 September 2021; Accepted 4 October 2021
Available online 9 October 2021
1059-1311/© 2021 British Epilepsy Association. Published by Elsevier Ltd. This article is made available under the Elsevier license (http://www.elsevier.com/open-
access/userlicense/1.0/).
B. Mikula et al.
has led researchers and clinicians to the notion that the detailed inves­
tigation of the social-cognitive domain and the identification of poten­
tial risk factors is urgently needed [11,12].
1.1. The concept, measurement, and neural bases of social cognition
Social cognition (SC) is one of the six core neurocognitive domains
according to the fifth edition of the Diagnostic and Statistical Manual of
Mental Disorders (DSM-5, [13]). It is a broadly used term for multiple
perceptual, emotional, and cognitive mechanisms related to social
functioning [14]. This complex set of abilities ranges from reading
emotions via facial expressions, through inferring behavior from mental
states, to engaging in real-life social interactions [15]. This complexity
manifests in different theoretical models and neuropsychological
assessment of SC, thus, the exact components of this construct are
differently specified. To date there has been little agreement on which
components are considered as parts of SC. Some authors consider the
perception of emotional signals from multiple modalities, e.g. from gaze
direction, facial expressions, posture, and prosody, a fundamental
component [14,16,17]. Experimental paradigms and neuropsychologi­
cal tests targeting emotion recognition (ER) require participants to choose
among labels based on a given emotional material, such as a visual
presentation of human facial expressions. The awareness that other
people have mental states (e.g. beliefs, desires) different from our own
and that their behavior can be explained by these mental states is
referred to as "theory of mind" (ToM, [18]). Besides abstract inferences,
automatic simulation of others’ inner states can also contribute to social
understanding [19]. The term “mentalizing” covers such spontaneous
mechanisms during human belief attribution [19]. Although SC en­
compasses several cognitive and non-cognitive aspects, in this review we
discuss only these two main components: ER and ToM. The term
social-cognitive skills will be used here to refer to these components.
Traditional neuropsychological tests of ToM focus on the ability to
reason about thoughts and feelings of fictive characters demonstrated
either verbally (e.g. by short written stories), visually (e.g. by cartoons),
or with the use of multimodal materials such as videos. All of these al­
ternatives depict social situations in which agents engage in interactions
and where the interpretation of the stories requires mental state attri­
bution. For instance, in the Faux pas recognition test (FPR), a frequently
used measure of ToM, participants have to detect socially awkward
comments in short written stories of everyday scenes [20]. The awkward
comments ¡ faux pas-s ¡ arise from misunderstandings or insufficient
knowledge of a character, who thus unintentionally hurts another
character’s feelings. With these behavioral paradigms, a considerable
amount of research has investigated the neural mechanisms of
social-cognitive processing.
It is now widely accepted that the neural system, also called the
‘social brain’ which subserves SC skills, comprises well-defined brain
regions and distributed networks interconnecting them [21]. According
to the neuroimaging literature, the amygdala, an essential part of the
limbic system, might be considered as a hub within the social brain, by
virtue of its widespread anatomical connections with regions implicated
in perceptual, cognitive, and motivational aspects of social functioning
[22]. Theory of mind is further associated with the temporo-parietal
junction [23] which is implicated in perspective-taking, and the
medial prefrontal cortex which has an important role in self-other dis­
tinctions and intention attribution [24]. It is also hypothesized that the
social network connecting these regions partially overlaps with the
default mode network, which involves additional nodes such as the
precuneus, posterior cingulum, and mediotemporal areas [25]. More­
over, core regions of social cognitive functioning are the superior tem­
poral sulcus, which shows activation for biological motion, social
interaction as well as communicative intent, and the temporal poles that
engage in social memory retrieval [26].
In the past thirty years, SC disturbances have gained growing
attention in the clinical fields, due to their high prevalence in certain
64
Seizure: European Journal of Epilepsy 93 (2021) 63–74
neurodevelopmental and psychiatric disorders [27]. It seems plausible
that many neurological conditions are accompanied by alterations in the
SC domain as well, hence testing these abilities could provide further
insight into the functional relevance of the potential deficits [28].
1.2. The broadening neurocognitive profile of TLE: social-cognitive
deficits
Temporal lobe epilepsy is now believed to be characterized by def­
icits in the social-cognitive domain, including both ER and ToM [10].
According to some, this pattern of dysfunction appears to be associated
with other cognitive functions, such as decision making [29] and
working memory [30], although the formal analysis of the possible in­
fluence of general cognitive status on SC is scarce across the literature.
Evidence from research targeting emotional perception suggests that
patients with TLE have difficulties in recognizing negative emotions,
especially fear [29,31,32]. However, the specific role of laterality re­
mains unclear: patients with right TLE show robust emotion recognition
deficit when compared to a healthy control group, but differences be­
tween right and left-sided patients are not consistently reported [33,34].
Besides diverse methodological approaches, the nature of the disease
may also contribute to the mixed results. The network approach of TLE
suggests that the disorder might be the dysfunction of the limbic system
which shows aberrant structural organization in patients with TLE [35].
On a functional level, the altered brain structure could manifest in dis­
rupted connectivity between parts of the limbic structures during
emotion perception [36]. Nevertheless, a recent study applying graph
theory indices by Huang and colleagues revealed that unilateral excision
of the amygdala in patients with left or right TLE did not influence the
characteristics of the emotion-processing network when it was
compared to normal controls [37]. In the advanced social-cognitive
domain, studies assessing SC with ToM tasks have come to similar
findings: patients with TLE perform poorer than their healthy counter­
parts. Using the FPR test a number of studies found a decline in ToM
abilities [29,31,38]. However, there is inconsistent evidence for the ef­
fect of laterality, since independent studies found patients with both left
[39] and right [38] TLE to be more impaired. Furthermore, it is also
reported that patients with TLE score lower on ToM measures with more
basic stimuli, such as the interpretation of biological motion in a social
context, or the attribution of intentionality to moving shapes [40,29,41].
These tasks with low cognitive load are ideal for exploring neural
changes during mental state attribution. In an imaging study, Hennion
and colleagues observed different patterns of brain activation between
patients with mTLE and healthy controls during the animated shapes
task [41]. While a hypo-activation in the precuneus and fusiform gyrus
was found in patients with right mTLE, they exhibited greater activation
in the cerebellum and dorsolateral prefrontal cortex compared to con­
trols when watching interactions of geometrical shapes with intentional
content.
There are probably several, interacting factors that underlie the
social-cognitive deficit in TLE. On one hand, psycho-social problems, for
instance, social isolation caused by more severe seizures, dependence on
family members, and the stigma surrounding people with epilepsy may
limit the opportunities for social interactions [1]. On the other hand, as
mentioned above, clinical characteristics of the disorder such as inter­
ictal epileptic brain activity [42] together with the involvement of
medial and lateral temporal areas which are part of core mentalizing
networks [43], can serve as an organic cause of the deficit. It has been
argued that a potential risk factor of ToM and ER impairment in TLE is
the age of seizure onset, suggesting a developmental impact of the dis­
order (see [10,33] for reviews). Importantly, it is not clear whether
epilepsy alone accounts for the impaired performance, or it emerges
selectively in TLE [44,45,46]. It has been already established that pa­
tients with frontal lobe epilepsy show a similar pattern of ToM
dysfunction [39], however, results appear to be mixed in other focal
epilepsies or generalized epilepsies [47,48].
B. Mikula et al.
In case of ineffective seizure control with antiepileptic drugs (AED)
and depending on the clinical characteristics (e.g. site of the epileptic
focus), epilepsy surgery allows for significant improvement in seizure
condition for patients. An extensive literature on cognitive outcomes
after surgical treatment of drug-resistant TLE has now been accumulated
[49]: problems with episodic memory [4] and naming [50] are the most
common cognitive deficits following the partial resection of the
language-dominant temporal lobe. This intervention often incorporates
the removal of the anterior temporal lobe, which receives considerable
input from several cortical regions, thus, serves as an ideal node for
integrating multimodal semantic or conceptual representations [51].
Concerning the social-cognitive domain, the anterior temporal lobe has
important connections with the amygdala and the orbitofrontal cortex
(OFC), consequently, it plays a role in both coding and storing
socio-emotional signals [52]. Nevertheless, there is little evidence for
the effect of surgical treatment on social-cognitive functions in TLE.
Tracking postoperative changes would be reasonable from both
psycho-social and neural perspectives [53]. First, a sudden shift in pa­
tients’ lifestyle due to seizure freedom elicits demands on social adap­
tation which can be challenging after a long period of social isolation
and dependence [54]. Second, neural structures targeted by standard
surgical protocols − the amygdala and the anterior temporal lobes −
show considerable overlap with core parts of the social network. Thus, it
can be hypothesized that resecting an essential part of the network
might result in the impairment of the SC domain, however, it is also
possible that directly manipulating a maladaptive network will promote
neural reorganization and cognitive recovery [33,55]. The results of
longitudinal studies in this field could provide further valuable infor­
mation for patients and physicians concerning the cognitive prognosis of
epilepsy surgery [40].
The aim of the present review is the qualitative synthesis of findings
on the ER and ToM skills of patients with drug-resistant TLE following
surgical treatment. Although these two components of the broad term SC
are the most frequently studied in TLE, to date, there is only a small
group of studies investigating this issue either in a cross-sectional
fashion or longitudinally. Results are discussed with special emphasis
on methodological heterogeneity and diagnostic considerations.
2. Methods
Searches were conducted with the use of the online databases
PubMed and Scopus as well as manual searches of references in relevant
papers. The review period was from 2000 to 2021. Records were
screened by the first author (B.M.) in April 2021. Articles were identified
by carrying out a comprehensive review of published research papers
that have focused on SC functions of surgically treated patients with
TLE. Search terms were ("temporal lobe epilepsy" OR ("temporal" AND
"lobe" AND "epilepsy")) AND ("social cognition" OR ("social" AND
"cognition") OR ("theory of mind" OR ("theory" AND "of" AND "mind"))
OR ("emotion")) AND ("surgery" OR "temporal lobectomy" OR ("tempo­
ral" AND "lobectomy”)). Studies were eligible if they (1) included pa­
tients with a diagnosis of TLE, (2) included a healthy comparison group,
(3) reported original research, (4) were published in peer-reviewed
journals and in English language, (5) reported the intervention of epi­
lepsy surgery. The abstracts and full papers were reviewed to remove
articles according to the following exclusion criteria: (1) case studies, (2)
studies that did not focus on social-cognitive abilities, (3) studies that
used interviews or self-report questionnaires to examine SC functions.
Imaging studies that investigated facial emotion processing or social
inference in TLE without explicit behavioral measures of these con­
structs during the task were also excluded.
The initial search identified 275 titles and abstracts. After removing
duplicates (n = 64), 211 titles and abstracts were screened, resulting in
the exclusion of 188 studies for the following reasons: written in non-
English language (n = 1), publication before 2000 (n = 13), lack of
healthy control group (n = 3), irrelevant research type (reviews, book
65
Seizure: European Journal of Epilepsy 93 (2021) 63–74
chapters, case studies, letters; n = 49), investigation of constructs other
than SC (n = 104), target group not being patients with TLE or non-
surgically treated patients with TLE (n = 14) and task type not investi­
gating ER or ToM explicitly (n = 5). Full texts of 22 papers were
screened, and additional 6 studies were excluded. In total 16 articles met
our inclusion criteria. Fig. 1 displays the flowchart of the selection
process.
Fig. 1 Flow diagram of the identification and selection process
3. Results
The description of study characteristics and main findings are sum­
marized in Table 1. The reviewed studies investigated several aspects of
the topic (e.g. multiple dependent variables, mixed design and cova­
riates). In order to promote understanding, we applied the following
subdivisions. Results of ER and ToM abilities and the two types of
methodological approaches (cross-sectional and longitudinal research)
are reported separately. Consequently, particular articles will be dis­
cussed in more than one subdivisions.
3.1. Emotion recognition
3.1.1. Cross-sectional studies
Most of the included studies investigated ER in a post-surgery group
of patients with TLE compared with either presurgical patients and
healthy participants [56–59] or healthy controls alone [60–66]. Nearly
all studies of the latter group confirmed that post-surgery patients with
TLE recognize emotional states less accurately from static pictures [61,
63,64,66] and dynamic expressions [60,59], as well as from musical
tones [62]. This deficit appears to be selective for negative emotions,
such as fear [60–63,66] and disgust [60,61,66]. With respect to positive
emotions − including happiness − a long-term follow-up study revealed
general ER impairment 8 years after temporal lobectomy [64]. Different
ER patterns can be associated with different surgical methods. Accord­
ing to a direct comparison between anterior temporal lobectomy (ATL)
and selective amygdalo-hippocampectomy (SAH), while patients with
ATL were impaired in fear recognition, patients with SAH had more
problems with identifying disgust [66]. Concerning general ER perfor­
mance, both patient groups performed below controls, and patients with
SAH were even more impaired than patients with ATL. In a functional
magnetic resonance imaging study, Van de Vliet and colleagues explored
the effect of amygdala resection on body emotion perception [65]. Their
results showed that patients with neither left nor right ATL had diffi­
culties with the explicit categorization of body emotions (happiness,
fear, sadness, anger and neutral) from moving puppets similar to
humans. Contrary, group differences were found on a neural level: pa­
tients with ATL had weaker brain activation for emotional movements
compared with healthy controls in a distributed network of cortical re­
gions. In addition, patients’ body responsive areas, the extrastriate body
area (EBA) and the posterior superior temporal sulcus (pSTS) responded
similarly to controls’ when distinguishing between emotional versus
neutral movements, except the right pSTS which categorized stimuli less
reliably in patients with right ATL than in controls. Within-group ana­
lyses showed that the discrimination of the four emotional categories
was below chance in EBA or pSTS among patients with left or right ATL,
respectively. However, group differences between patients and controls
did not achieve significance.
Comparison between separate groups of presurgical and postsurgical
patients indicates that ER performance is mostly independent of surgical
status [56,58,59]. Recognizing fear seems to be challenging both before
and after surgery [58,59], while there is some evidence that happiness
recognition can be better postoperatively [57,58]. Grouping patients
according to both surgical status and laterality offers the opportunity to
make clinically more relevant claims regarding postoperative ER.
Interestingly, when measured with short video clips, only ER abilities of
patients with right ATL did not differ from controls, the remaining
B. Mikula et al.
Fig. 1. PRISMA 2020 flow diagram of identification and selection of studies.
patient groups (left ATL, right TLE, left TLE) had difficulties in the
identification of at least one emotional state [57].
3.1.2. Longitudinal studies
Longitudinal studies on the effect of surgery show mixed results: two
studies found a difference in ER before and after surgery [67,55], while
another study reported comparable pre- and postoperative performance
[56]. Benuzzi and colleagues investigated facial ER among 6 patients
with TLE (4 right-sided) and found a decreased ability to recognize fear
only in patients with early-onset right TLE prior to surgery [67]. These
patients exhibited significant improvement after surgery and recruited
the same brain regions as healthy participants when watching fearful
facial expressions: the left OFC and the extrastriatal cortices bilaterally.
Since this activation was fully absent preoperatively, the authors suggest
that removing the lesioned medio-temporal structures enables func­
tional reorganization in early-onset mTLE [67]. With a complex ER task,
others found impaired emotion discrimination for all basic emotions in
right TLE except for happiness and ATL did not influence this pattern
[55]. Contrary, patients with left TLE showed better postoperative
discrimination for fear, however, their performance did not differ from
controls preoperatively. Here, patients had to rate the intensity of each
66
Seizure: European Journal of Epilepsy 93 (2021) 63–74
basic emotion (happiness, fear, surprise, anger, disgust and sadness)
from photographs of facial expressions. The discrimination index was
calculated on the basis of congruent (e.g. maximal fear rating for a
fearful expression) and incongruent (e.g. 30% fear rating for a surprised
expression) responses. In a third study, although there was a lack of
change on a group level with respect to ER from static facial expressions,
a subgroup of patients showed either deterioration (n = 7) or
improvement (n = 5) after surgery [56].
3.1.3. Clinical variables: side of surgery, disease onset and duration,
etiology
Presumably, the age of epilepsy onset affects the degree of ER
dysfunction in patients with ATL. Earlier onset is associated with lower
fear recognition, especially after right ATL [61,58,63], however, the
opposite pattern has also been observed [64]. Regarding etiology, Cohn
and colleagues found that patients with ATL whose preoperative lesion
was left mediotemporal sclerosis (MTS) performed below presurgical
patients with the same etiology on general ER [57]. In most cases, the
restricted sample size of the longitudinal studies did not make it possible
to analyze group differences with regard to laterality. In spite of this,
preliminary evidence suggests that patients with either left [55] or right
 B. Mikula et al.
Table 1
Cross-sectional and longitudinal studies of social cognition after temporal lobe epilepsy surgery.
Study Study design Groups Age Onset Duration IQ Preop. Surgery type Postop. Constructs (measures) Results
(mean, (mean, (mean, SD (mean, measurement measurement
SD or SD in in years) SD or point (years) point (years)
range in years) range)
years)

Anderson Cross- TL NR VIQ; - Approximate 3.5-cm resection 2-8 FER (rating the lTL = HC > rTL; Fear, disgust,
et al. sectional (n=23) PIQ of the anterior middle and appropriateness of 6 basic happiness rTL<lTL; Facial emotion
(2000) 11 lTL 32 (8) 6.2 (5) 91 (12); inferior temporal gyri and facial emotional evaluation impairment is
99 (14) subsequent removal of 70-80% expressions on the basis associated with early seizure onset
12 rTL 38 (8) 6.7 (7) 97 (12); of the amygdala and all of the of emotional labels) in rTL
102 (15) hippocampus,
23 HC 38 (8) parahippocampus
Gosselin Cross- TL NR NR - Medial temporal lobe 1.2-8.3 ER from instrumental Scary: lTL = rTL < HC; Peaceful:
et al. sectional (n=16) resection, including the whole music (fear, peacefulness, lTL = rTL < HC; Most ambivalent
(2005) 8 lTL 40.5 (29- 94 (79- amygdala as well as various happiness, sadness) responses to scary music in the two
47) 114) amounts of the hippocampus TL groups; No group differences
8 rTL 40.3 (30- 98 (79- and surrounding cortices observed in happy and sad music;
60) 112) (entorhinal, perirhinal and Lower arousal ratings for both
16 HC 38.6 (27- parahippocampal cortex) peaceful (lTL) and scary (rTL)
47) music in patients
Schacher Cross- MTLE - ATL or SAH 1-4 ToM (FPR) ToM; ATL- = ATL+ < HC = Extra
et al. sectional (n=27) MTLE; No differences between pre-
(2006) 16 ATL- 35 (12) 14.7 20 (14.8) 110 (13) and postop. patients with mTLE;
(13) Lower FPR performance in rTLE in
11 ATL+ 38.5 12 (9.2) 25.8 (12) 103 (21) the whole group (ATL+, ATL-)
(8.5)
67

Extra 35.9 (13) 15.6 20.3 (15) 109.5

MTLE (14) (16.4)
(n=27)
12 HC 33.8 (12) 120
(11.3)
McClelland Cross- rATL NR NR - Non-dominant ATL 5 FER (fear, anger, Fear: Early-onset TLE<HC; Late-
et al. sectional (n=12) happiness) onset TLE = HC; Early-onset
(2006) 7 early- <6 TLE<Late onset TLE (p>.05);
onset Anger:; All p values >.05;
5 late- >5 Happiness: All p values >.05;
onset Disease onset is not associated
10 HC 30.4 with the severity of FER deficit
within TLE groups
Shaw et al. Longitudinal TLE NR VIQ; 0.1-0.3 En bloc anterior temporal lobe 0.4-0.6 Facial emotion Preop. Discrimination index: rTLE

Seizure: European Journal of Epilepsy 93 (2021) 63–74

(2007) (n=19) PIQ resection discrimination (Ekman); < HC (except happiness); lTLE <
10 rTLE 41(9) 26(16) 97(18); ToM (Strange stories, HC (only sadness); ToM:;
98 (20) FPR); EF (Brixton and rTLE = lTLE = HC; Postop.
9 lTLE 33 (11) 26 (33) 102 Hayling tests) Improvement in fear
(18); 98 discrimination after left ATL; ToM:
(12) rTLE = lTLE = HC; Change in EF
19 HC 33 (11) 112 (6); did not correlate with change in
112 (15) ToM
Ammerlaan Cross- NART- - Unilateral amygdalo- 1.5 (0.4) ER (Emotion Recognition Patients with TLE recognized fear
et al. sectional IQ hippocampectomy Task); Interpersonal (above 80%) and disgust (above
(2008) TLE 37.1 19.9 18 (10.4) 94.1 behavior (Scale for 65%) on higher intensities than HC
(n=9) (3.4) (12.8) (4.5) Interpersonal Behavior); (above 60% and 50%,
5 rTLE Facial perception (Benton respectively); No differences
4 lTLE Test of Facial Perception); between subjective interpersonal
14 HC Depression (BDI) behavior; No differences in facial
(continued on next page)
 B. Mikula et al.
Table 1 (continued )
Study Study design Groups Age Onset Duration IQ Preop. Surgery type Postop. Constructs (measures) Results
(mean, (mean, (mean, SD (mean, measurement measurement
SD or SD in in years) SD or point (years) point (years)
range in years) range)
years)

36.4 107.6 perception and depressive

(3.4) (3.3) symptoms
Hlobil et al. Cross- TLE NR - Standard ATL >1 FER (fear, anger, FER; Happiness: ATL- <
(2008) sectional (n=76) happiness) ATL+ = HC; Fear: ATL- = ATL+ <
ATL- HC; Anger: ATL- = ATL+ Earlier
(n=36) onset in rATL- and rATL+ is
24 rATL- 28.8 (11) 21.5 96 (15) associated with lower fear
(12.7) recognition
12 lATL- 29.5 18.7 (6) 95 (16)
(7.4)
ATL+
(n=40)
21 33.4 (10) 21.8 97 (14)
rATL+ (11.7)
19 30 (11.7) 15 (8.3) 94 (13)
lATL+
28 HC 31 (12.3)
Tanaka et al. Cross- MTLE NR - ATL or SAH NR FER (dynamic stimuli) FER from dynamic facial
(2013) sectional (n=88) expressions; Fear: PTL = TL- < HC;
25 TL 41.5 (33- Disgust: TL- < HC; Sadness: PTL <
60) HC; No differences in recognition
11 rTL 11.8 26.6 of happiness, surprise, and anger
(6.7) (11.6)
68

14 lTL 14 25.4
(10.4) (14.5)
63 MTLE 43 (28.8-
58)
17 26.4 16.8
rMTLE (20) (12.6)
26 28.4 14 (12)
lMTLE (20)
20 37.7 8.6 (15.5)
bilateral (25)
32 HC 33 (26-
47)
Benuzzi et al. Longitudinal MTLE 23.2 NR NR NR 0.6 NR 0.6 FER; Change in brain Preop.2 rMTLE < HC (fear, anger/

Seizure: European Journal of Epilepsy 93 (2021) 63–74

(2014) (n=6) activation for fearful faces surprise/sadness); fMRI for fearful
4 rMTLE faces; lateral PFC, OFC,
2 lMTLE extrastriate cortex; HC > 2 rMTLE;
6 HC 36.8 Postop.; rMTLE = HC; fMRI for
fearful faces; lateral PFC, OFC,
extrastriate cortex; HC = 2 rMTLE
Amlerova Cross- TLE NR FISQ NR Temporal resection the extent >1 FER (Ekman 60 Faces); Preop. FER:; ATL- = ATL+ < HC;
et al. sectional (n=74) of which did not extend ToM (FPR) Preop. ToM: ATL- = ATL+ < HC;
(2014) 22 rTLE 41 (11) 23 (16) 97 (16) beyond the temporal lobe, and Postop.; No group-level differences
15 rATL 35 (8) 19 (11) 100 (13) included at least part of mesial in ToM or FER; Changes are not
24 lTLE 33 (10) 18 (9) 97 (14) temporal lobe structures associated with clinical variables;
13 lATL 33 (7) 10 (7) 94 (19) Lower IQ predicts FER and ToM
20 HC 33 (13) 108 (14) dysfunction in the whole group of
Longitudinal TLE patients
(n=30)
(continued on next page)
 B. Mikula et al.
Table 1 (continued )
Study Study design Groups Age Onset Duration IQ Preop. Surgery type Postop. Constructs (measures) Results
(mean, (mean, (mean, SD (mean, measurement measurement
SD or SD in in years) SD or point (years) point (years)
range in years) range)
years)

Meletti et al. Cross- ATL 45.3 (11) 15.3 21.2 91.6 - Extended temporal; lobectomy 8.5 (2.5) FER, rating the intensity, FER; For all emotional categories:
(2014) sectional (n=42) (12) (13.4) (13.3) (N=30) and anteromedial valence and arousal of ATL < HC; Intensity:; ATL = HC;
21 rATL temporal lobectomy (N= 12) emotions Arousal:; Lower intensities for fear,
21 lATL disgust, anger and neutral in ATL;
39 HC 44 (15) Valence: Lower ratings for all
emotional categories except
happiness in ATL; Earlier onset
(<6 years) is associated with fewer
errors in fear recognition; Side of
ATL does not impact performance
Wendling Cross- TLE - SAH vs. standard TL FER (Ekman 60 Faces); FER; General: SAH < ATL; Fear:
et al. sectional (n=60) Depression (BDI); Psycho- ATL < SAH = HC; Disgust: SAH <
(2015) 27 SAH 41.4 12.1 25.4 89.2 6.9 (2.8) pathology (SCL-90-R) ATL = HC; Surprise: left surgery <
(8.3) (11) (13.2) (17.6) HC irrespective of method; All ps >
33 ATL 40.1 11.8 27 (13.5) 87.1 8.1 (2.8) .05 for happiness, sadness and
(9.2) (11) (22) anger; No correlation observed
30 HC 40.6 between FER and depression/
(4.8) psychopathology
Cohn et al. Cross- TLE FISQ - In 30 patients, standard en bloc >0.6 ER (TASIT); Social ER; Anxiety: lTLE, lATL < HC;
(2015) sectional (n=50) excisions removing; 4.5 cm of inference from complex, Disgust: lTLE, lATL < HC;
26 rTLE 38 (13) 18 (13) 19 (15) 102 (12) the anterior inferior and dynamic videos: sarcasm Happiness: rTLE < HC; Anger:
24 lTLE 39 (12) 22 (13) 16 (14) 107 (11) middle temporal gyri.; Seven and lie comprehension lATL < HC; Sincere exchanges: All
ATL additional patients had a more (TASIT) patient groups = HC; Sarcasm:;
69

(n=37) restricted neocortical resection rTLE < HC; lATL < HC; rATL <
19 rATL 39 (9) 16 (13) 20 (12) 105 (8) HC; lATL < lTLE; Lie: All patient
18 lATL 42 (13) 16 (16) 24 (18) 102 (12) groups = HC; Sarcasm and deceit
15 HC 38 (8) comprehension is associated with
disease onset and MTS in the
whole group
Giovagnoli Longitudinal TLE RCPM NR ATL up to 6.5 cm of the 1 ToM (FPR); Naming Preop. FPR Total: early and late-
et al. (n=85) (0-36) anterior lateral non-dominant (BNT); Planning (ToL); onset TLE < HC; FPR Correct
(2016) 31 early- 31.9 5.9 (3.8) 26 (10.8) 31 (3.8) temporal lobe and up to 4.5 cm Episodic memory (Short rejection: early-onset TLE < late-
onset < (9.4) of the dominant temporal lobe; story) onset TLE = HC; FPR Recognition:
12 years MTL resection encompassed early- and late-onset TLE < HC;
14 lTLE the uncus, amygdala, and the Naming: rTLE = lTLE < HC;
17 rTLE rostral 1–3 cm of the Planning: early-onset TLE < late-

Seizure: European Journal of Epilepsy 93 (2021) 63–74

54 late- 34.9 23.7 11.4 (8.5) 33(2.7) hippocampus onset TLE = HC; Memory:
onset (10.2) (8.5) rTLE = lTLE < HC; Postop.; FPR
>12 Total: no change in either TLE
years group; FPR Correct rejection:
25 lATL improvement only in early-onset
29 rATL TLE; FPR Recognition: no change
40 HC 36 (9.6) 33 (3.9) in either TLE group; Naming: rTLE
improvement, lTLE decline;
Planning: improvement only in
early-onset TLE; Memory: lTLE <
rTLE but no interactions;
Predictors of postop. performance:
preop. level of ToM, postop. IQ,
number of AEDs, level of education
NR NR - ATL or SAH 10.5 (0.9)
(continued on next page)
 B. Mikula et al.
Table 1 (continued )
Study Study design Groups Age Onset Duration IQ Preop. Surgery type Postop. Constructs (measures) Results
(mean, (mean, (mean, SD (mean, measurement measurement
SD or SD in in years) SD or point (years) point (years)
range in years) range)
years)

Van de Vliet Cross- ATL ER from body motion Explicit categorization of body
et al. sectional (n=20) (happiness, anger, fear, emotions: ATL = HC; Brain
(2018) 10 rATL 52.3 (11) 13 (9.8) sadness, neutral); Brain activation for emotional vs.
10 lATL 52.3 (8) activation changes for neutral stimuli; EBA:
12 (11.5) body emotions rATL = lATL = HC; Right pSTS:
rATL < lATL = HC; Brain
activation for emotion
categorization; rATL = lATL = HC
12 HC 54.3 (8)
Bala et al. Cross- TLE ATL- 33.1 12.9 20.2 NR - ATL 4.3 (3.3) Mental state attribution Frith-Happé animations: ATL-,
(2018) sectional (n=21) (11.4) (10.5) (11.9) to moving shapes and ATL+ < HC in goal-directed and
10 rATL- point-light displays mentalizing action identification;
9 lATL- (Frith-Happé animations ATL+ < HC in emotion attribution
TLE 35.9 11.5 22.8 (9.7) and CID-5); EF; to shapes subtask; CID-5 biological
70

ATL+ (6.8) (9.4) Processing speed motion: ATL-, ATL+ < HC in

(n=19) individual movement
11 identification; rATL+ < lATL+ in
rATL+ communication identification;
8 lATL+ Effects remained significant after
20 HC 30.2 controlling for years of education;
(11.5) Association with clinical, cognitive
and demographic variables were
measured only in a unified TLE
group

Abbreviations: AEDs antiepileptic drugs, ATL anterior temporal lobectomy, BNT Benton Naming Test, EBA extrastriate body area, EF executive functions, ER emotion recognition, FER facial emotion recognition, FPR faux
pas recognition test, FSIQ Full-scale IQ, HC healthy controls, lATL left anterior temporal lobectomy, lMTLE left mediotemporal lobe epilepsy, lTLE left temporal lobe epilepsy, MTLE mediotemporal lobe epilepsy, NART

Seizure: European Journal of Epilepsy 93 (2021) 63–74

National Adult Reading Test, NR not reported, OFC orbitofrontal cortex, PFC prefrontal cortex, PIQ Performance IQ, postop. postoperative, preop. preoperative, pSTS posterior superior temporal sulcus, rATL right anterior
temporal lobectomy, RCPM Raven’s Coloured Progressive Matrices, rMTLE right mediotemporal lobectomy, rTLE right temporal lobe epilepsy, SAH selective amygdalo-hippocampectomy, TL temporal lobectomy, TL-
before temporal lobectomy, TL+ after temporal lobectomy, TLE temporal lobe epilepsy, ToL Tower of London test, ToM theory of mind, VIQ verbal IQ.
B. Mikula et al.
[67] TLE have the potential to improve in ER following surgery. Addi­
tionally, early seizure onset and lower preoperative functioning might
be associated with postoperative enhancement [67]. Nonetheless,
changes in performance after surgery are not always associated with any
clinical variable [56].
3.2. Theory of mind
3.2.1. Cross-sectional studies
In total, 4 studies had investigated ToM abilities in a cross-sectional
design [56,40,57,45]. Neither of these studies showed any difference in
mental state attribution between presurgical and postsurgical patients
with TLE. This finding was established with different experimental
methods. In two cases, the shortened version of the FPR test was used to
evaluate ToM reasoning [56,45]. Patients before and after epilepsy
surgery were found to be impaired as opposed to healthy participants,
however, the two patient groups had comparable performance. Others
administered “The Awareness of Social Inference Test” (TASIT), an
ecologically valid measure of ToM reasoning and pragmatic abilities
[57]. The task encompasses sub-tests of ER as well as sarcasm and lie
comprehension, each examined with short video clips of everyday social
situations. As for higher-order SC, none of the patient groups (left and
right ATL, left and right TLE) exhibited deficits in the comprehension of
sincere and deceitful exchanges. In contrast, the interpretation of
sarcastic dialogues in which the content and the context are incon­
gruent, all patient groups scored lower than controls, except for patients
with left TLE. The only significant difference between pre- and post­
operative groups occurred in this subtest: patients with left ATL per­
formed poorer than patients with left TLE. Applying more simplistic
stimulus materials, Bala and colleagues concluded that patients with and
without temporal lobectomy performed comparably on mental state
attribution tasks [40]. They used two separate tasks to measure men­
talizing ability: one showed moving geometrical shapes, and the other
included point-light displays that imitated either communicative or in­
dividual human biological motion. Regardless of surgery, patients with
TLE were found to be less effective when they had to categorize
goal-directed or mentalizing interactions of geometrical shapes as
compared to random motion. Moreover, only patients after ATL per­
formed below healthy controls on the emotion attribution part of the
mentalizing animations: that is, they misinterpreted the underlying
emotion of a target figure. Similarly, the pre- and postsurgical groups
were equally impaired on the interpretation of point-light motion of two
agents. Surprisingly, patients with TLE incorrectly recognized individual
actions as communicative more often than controls.
3.2.2. Longitudinal studies
In general, longitudinal data suggest that higher-order SC is unaf­
fected by epilepsy surgery. According to two independent studies, ToM
inferential abilities measured with the FPR test remain stable 6–12
months after surgery [56,55]. In a large cohort of patients (n = 84),
Giovagnoli and colleagues found decreased initial performance but
greater postoperative enhancement in the correct rejection of faux pas-s
only in the early-onset TLE group (< 12 years), suggesting that the
“worse the preoperative deficit, the greater the postoperative gain” [68].
Conversely, irrespective of disease onset, patients had problems with the
identification of existing faux pas-s preoperatively, and this pattern was
not affected by surgery. It is important to note, however, that the
follow-up of the healthy control group was accomplished in only one
study [55], the lack of which makes the interpretation of longitudinal
data ambiguous.
3.2.3. Clinical variables: side of surgery, disease onset and duration,
etiology
Some of the cross-sectional studies combined pre- and postsurgery
patients when analyzing the effects of clinical variables. In such a
combined group, Cohn and colleagues found that individuals with the
71
Seizure: European Journal of Epilepsy 93 (2021) 63–74
preoperative lesion of MTS had more pronounced deficits in ToM
compared to patients with other etiologies or with MRI-negative TLE
[57]. Moreover, patients with left ATL and presurgical MTS performed
below patients with left TLE and MTS in sarcasm comprehension. Others
reported that patients with right ATL had more difficulties identifying
communicative actions of point-light displays than patients with left
ATL [40]. Longitudinally, significant predictors of postoperative ToM
performance were the preoperative level of ToM and the number of
AEDs [68]. While preoperative performance was affected by laterality,
no differences were found between left and right ATL postoperatively
[68].
3.2.4. General cognition
As mentioned previously, it is yet to be explored whether impair­
ments in general cognitive skills contribute to SC performance in TLE.
Although most of the reviewed studies (11 of 16) reported IQ scores,
only 3 had significant results regarding intelligence and SC in this
population. Given the equal performance, 2 studies comparing pre-and
postsurgical patients analyzed the moderating variables in a combined
group of patients and found that the level of intelligence was related to
the variability in ER and ToM scores [56,45]. Longitudinally, post­
operative IQ, and the level of education seemed to have an effect on
postoperative ToM abilities [68]. In addition, changes in executive
functions were not associated with changes in ToM performance
measured by the FPR and the Strange Stories test [55].
4. Discussion
There is now an increasing volume of studies describing the social-
cognitive profile of TLE. It has been consistently reported that in­
dividuals with TLE show deficits in both basic and higher-order SC,
including ER [34] and ToM [10]. For patients who experience recurring
seizures despite antiepileptic medication, surgery can be an effective
treatment option. However, due to psycho-social and neurobiological
causes, this intervention might imply further changes in social-cognitive
functioning. The aim of the present review was to summarize findings on
social-cognitive skills of surgically treated patients with TLE. Both
cross-sectional and longitudinal studies were evaluated. Emotion
recognition deficits, especially for negatively valenced emotions, were
evident when the postsurgical group was contrasted with healthy con­
trols [60–64,66], but independent groups of pre-and postsurgical pa­
tients did not differ in terms of ER [56,58,59]. Only one study found
comparable performance in explicit ER between healthy participants
and patients after temporal lobe resection [65]. However, it can be
assumed that the type of measurement may have affected this pattern of
finding since ER was assessed with body emotions of artificial moving
puppets, in contrast with the majority of studies using human faces.
Concerning higher-order SC, only one domain was found to be impaired
in a cross-sectional comparison after left-sided surgery, namely the
interpretation of sarcasm [57]. With the same task, previous studies
found similar deficits in other neurological conditions, including de­
mentia [69] and multiple sclerosis [70]. With respect to the FPR test, the
most commonly used task to assess ToM abilities in this patient group,
the uniform finding is that in terms of total scores, surgery does not
affect ToM in either direction [56,68,55]. In sum, from a neurobiological
perspective, it is not yet clear whether temporal lobe excisions have a
greater impact on ER and ToM than the underlying brain pathology or
the maladaptive epileptic network.
4.1. Methodological heterogeneity
Taken together, firm conclusions from the reviewed literature can
not be drawn on the impact of epilepsy surgery with regard to basic and
higher-order social-cognitive functions, which may arise from substan­
tial methodological heterogeneity. The FPR is a commonly used measure
for observing ToM performance before and after surgery, although the
B. Mikula et al.
inconsistent administration of the test makes it difficult to contrast the
results of independent studies. While in earlier studies [56,45], a
shortened version was administered, which did not contain control
stories without faux-pas-s, the most recent longitudinal study [68]
applied the full version of the task and found postoperative changes in
the correct rejection of faux-pas-s exactly in these control stories. This
may indicate an overinterpretation of the stories: early-onset patients
reported that someone told something awkward even if there were no
faux pas-s in the story. Interestingly, a similar response bias was
observed when patients (both before and after surgery) had to categorize
point-light biological motion of two agents to be individual or commu­
nicative [40]. Patients were inclined to choose communicative labels for
individual actions more often than controls.
As can be seen in Table 1., the range of postoperative testing points is
extremely wide: re-testing occurred between 0.4–10 years after surgery.
Individuals who are contacted several years after the intervention may
be in an entirely different social position due to employment and the
expanding social network surrounding them, thus, they have already
had the opportunity to train social-cognitive skills. Contrary, cognitive
functioning in the first 6 months after surgery might be affected by acute
changes and potential mood disturbances related to the intervention
[71]. Thus, more multiple assessment follow-up studies with at least two
time points are needed to reveal the possible effect of time since surgery
on social-cognitive performance [53].
Furthermore, a limitation of the existing longitudinal literature is the
lack of postoperative testing in the healthy control group in the majority
of the studies. This design allows the authors to make claims about
changes only within the TLE group, however, some factors may impact
performance among healthy participants as well. For example, using the
same measures at pre- and postoperative assessment generates famil­
iarity, thus, reduces the validity of the observation [71]. In fact, none of
the longitudinal studies reported that alternative versions of the same
tasks were used, and only one paper mentioned this as a limitation [55].
Finally, the lack of any postsurgical effects should be considered in light
of the studies’ small sample sizes. None of the presented studies calcu­
lated power analyses prior to experiments, thus, it is possible that the
applied experimental design could tap large effects only. Future longi­
tudinal investigations may benefit from larger sample sizes, and the
involvement of a patient group with TLE awaiting surgery as a second
control group could also provide more definitive evidence.
4.2. Clinical implications
Due to the inconsistency in findings on the predictive value of clin­
ical, demographic and cognitive factors regarding social-cognitive
functions, the special role of testing SC prior to surgery is yet to be
clarified. Nevertheless, there is some evidence that is indicative of the
everyday relevance of SC for patients. A previous study revealed that
ToM performance in patients with TLE and frontal lobe epilepsy pre­
dicted quality of life perception, coping strategies and self-rated cogni­
tive functioning, suggesting that the better the ToM abilities, the better
these subjective indices [72]. Furthermore, performance on standard
ToM tasks, together with psychological status, but not seizure-related
clinical variables were associated with self-reported functional
outcome measures, such as interpersonal relationships and communi­
cation among presurgical patients with TLE [73]. Identifying associa­
tions with epilepsy-related factors, such as laterality, site of the lesion,
epilepsy onset and duration, number of AEDs and seizure frequency
would be an essential step towards the identification of patient clusters
at risk of postoperative SC difficulties. Early seizure onset is assumed to
be predictive of ER and ToM dysfunction, hence, some studies have
divided patients into two groups based on a cut-off point of age, e.g., 5 or
12 years, and compared early- versus late-onset patients [68,63].
Dichotomizing continuous variables (e.g. age at onset), albeit frequent
in clinical research, leads to information loss and reduced statistical
power [74]. The comprehensive presurgical evaluation of TLE relies on
72
Seizure: European Journal of Epilepsy 93 (2021) 63–74
multidisciplinary assessments, among which neuropsychological ex­
amination contributes equally to seizure lateralization and localization
[71]. Although social-cognitive functions have a distributed rather than
localized neural background [25], consistent associations between
certain tasks and activity of brain regions have already been established
[14,26]. The use of more simplistic stimuli such as moving geometrical
shapes and human biological motion in Bala and colleagues’ study rules
out linguistic demands, thus, decreases the effect of other cognitive
factors on performance [40]. Moreover, it has been shown that brain
regions being active during the interpretation of communicative ges­
tures and interactive intentions are the lateral temporal areas, namely
the superior temporal sulcus [75]. Consequently, patients who have
difficulties with identifying the social context behind these simplistic
displays are probably those whose lesion/focus is in the lateral temporal
lobe rather than in the mediotemporal areas.
Surgical intervention is an effective but irreversible treatment op­
tion, which may have a long-term impact on cognitive functioning,
especially when seizures are not fully controlled [76]. Despite the
well-established cognitive consequences of epilepsy surgery, there are
surprisingly few rehabilitation programs available for this population
[77].
The present review is limited in a number of ways. First, articles were
screened by only one author (B.M.), hence, we can not exclude the
possibility that relevant articles were overlooked. Second, searching in
databases other than PubMed and Scopus (e.g. Web of Science, Google
Scholar) would have allowed the identification of more studies. Third,
this paper does not summarize quantitative data from the original
studies, thus, it is not informative with respect to effect sizes. And fourth,
objective quality rating of the included studies was not carried out,
although the demonstration of strengths and weaknesses on the basis of
predefined criteria specific to this research area would have provided
further guidance for the interpretation of results.
5. Conclusions
In conclusion, the literature suggests that although SC dysfunction
reflected by altered ER and ToM is present in patients with TLE, surgical
treatment does not further deteriorate these skills. Nevertheless, longi­
tudinal results indicate that group-level comparisons may hide indi­
vidual decline or improvement. Follow-up investigations should be
complemented by adequate neuropsychological measures suitable for
multiple assessments as well as the retest of the healthy control group.
Declaration of Competing Interest
None.
Acknowledgements
GD was supported by the János Bolyai Research Scholarship of the
Hungarian Academy of Sciences. The authors would like to thank Réka
Schvajda and Boglárka Drubina for their valuable feedback on the
manuscript.
References
[1] Steiger BK, Jokeit H. Why epilepsy challenges social life. Seizure 2017;44:194–8.
https://doi.org/10.1016/j.seizure.2016.09.008.
[2] Bernhardt BC, Hong S, Bernasconi A, Bernasconi N. Imaging structural and
functional brain networks in temporal lobe epilepsy. Front Hum Neurosci 2013;7.
https://doi.org/10.3389/fnhum.2013.00624.
[3] Scheffer IE, Berkovic S, Capovilla G, Connolly MB, French J, Guilhoto L, Hirsch E,
Jain S, Mathern GW, Moshé SL, Nordli DR, Perucca E, Tomson T, Wiebe S, Zhang Y-
H, Zuberi SM. ILAE classification of the epilepsies: position paper of the ILAE
Commission for Classification and Terminology. Epilepsia 2017;58(4):512–21.
https://doi.org/10.1111/epi.13709.
[4] Bell B, Lin JJ, Seidenberg M, Hermann B. The neurobiology of cognitive disorders
in temporal lobe epilepsy. Nature Rev Neurol 2011;7(3):154–64. https://doi.org/
10.1038/nrneurol.2011.3.
B. Mikula et al.
[5] Viskontas IV, McAndrews MP, Moscovitch M. Remote Episodic Memory Deficits in
Patients with Unilateral Temporal Lobe Epilepsy and Excisions. The J Neurosci
2000;20(15):5853–7. https://doi.org/10.1523/JNEUROSCI.20-15-05853.2000.
[6] Stretton J, Thompson PJ. Frontal lobe function in temporal lobe epilepsy. Epilepsy
Res 2012;98(1):1–13. https://doi.org/10.1016/j.eplepsyres.2011.10.009.
[7] Bartha-Doering L, Trinka E. The interictal language profile in adult epilepsy.
Epilepsia 2014;55(10):1512–25. https://doi.org/10.1111/epi.12743.
[8] Hwang G, Dabbs K, Conant L, Nair VA, Mathis J, Almane DN, Nencka A, Birn R,
Humphries C, Raghavan M, DeYoe EA, Struck AF, Maganti R, Binder JR,
Meyerand E, Prabhakaran V, Hermann B. Cognitive slowing and its underlying
neurobiology in temporal lobe epilepsy. Cortex 2019;117:41–52. https://doi.org/
10.1016/j.cortex.2019.02.022.
[9] Reyes A, Kaestner E, Ferguson L, Jones JE, Seidenberg M, Barr WB, Busch RM,
Hermann BP, McDonald CR. Cognitive phenotypes in temporal lobe epilepsy
utilizing data- and clinically driven approaches: moving toward a new taxonomy.
Epilepsia 2020;61(6):1211–20. https://doi.org/10.1111/epi.16528.
[10] Bora E, Meletti S. Social cognition in temporal lobe epilepsy: a systematic review
and meta-analysis. Epilepsy & Behavior 2016;60:50–7. https://doi.org/10.1016/j.
yebeh.2016.04.024.
[11] Wilson SJ, Baxendale S, Barr W, Hamed S, Langfitt J, Samson S, Watanabe M,
Baker GA, Helmstaedter C, Hermann BP, Smith M-L. Indications and expectations
for neuropsychological assessment in routine epilepsy care: report of the ILAE
Neuropsychology Task Force, Diagnostic Methods Commission, 2013–2017.
Epilepsia 2015;56(5):674–81. https://doi.org/10.1111/epi.12962.
[12] Witt J-A, Helmstaedter C. Cognition in epilepsy: current clinical issues of interest.
Curr Opin Neurol 2017;30(2):174–9. https://doi.org/10.1097/
WCO.0000000000000430.
[13] Association American Psychiatric. Diagnostic and statistical manual of mental
disorders fifth edition. American Psychiatric Publishing; 2013.
[14] Adolphs R. Cognitive neuroscience of human social behaviour. Nature Rev
Neurosci 2003;4(3):165–78. https://doi.org/10.1038/nrn1056.
[15] Frith CD, Frith U. Implicit and Explicit Processes in Social Cognition. Neuron 2008;
60(3):503–10. https://doi.org/10.1016/j.neuron.2008.10.032.
[16] Cassel A, McDonald S, Kelly M. Establishing ‘proof of concept’ for a social
cognition group treatment program (SIFT IT) after traumatic brain injury: two case
studies. Brain Inj 2020. https://doi.org/10.1080/02699052.2020.1831072.
[17] McDonald S. New frontiers in neuropsychological assessment: Assessing social
perception using a standardised instrument, The Awareness of Social Inference
Test. Aust Psychol 2011;47(1):39–48. https://doi.org/10.1111/j.1742-
9544.2011.00054.x.
[18] Premack D, Woodruff G. Does the chimpanzee have a theory of mind? Behavioral
and Brain Sci 1978;1(4):515–26. https://doi.org/10.1017/S0140525X00076512.
[19] Frith CD, Frith U. The Neural Basis of Mentalizing. Neuron 2006;50(4):531–4.
https://doi.org/10.1016/j.neuron.2006.05.001.
[20] Stone VE, Baron-Cohen S, Knight RT. Frontal Lobe Contributions to Theory of
Mind. J Cogn Neurosci 1998;10(5):640–56. https://doi.org/10.1162/
089892998562942.
[21] Adolphs R. The social brain: neural basis of social knowledge. Annu Rev Psychol
2009;60(1):693–716. https://doi.org/10.1146/annurev.psych.60.110707.163514.
[22] Bickart KC, Dickerson BC, Feldman Barrett L. The amygdala as a hub in brain
networks that support social life. Neuropsychologia 2014;63:235–48. https://doi.
org/10.1016/j.neuropsychologia.2014.08.013.
[23] Carter RM, Huettel SA. A nexus model of the temporal–parietal junction. Trends
Cogn Sci (Regul. Ed.) 2013;17(7):328–36. https://doi.org/10.1016/j.
tics.2013.05.007.
[24] Amodio DM, Frith CD. Meeting of minds: the medial frontal cortex and social
cognition. Nature Rev Neurosci 2006;7(4):268–77. https://doi.org/10.1038/
nrn1884.
[25] Mars RB, Neubert F-X, Noonan MP, Sallet J, Toni I, Rushworth MFS. On the
relationship between the “default mode network” and the “social brain. Front Hum
Neurosci 2012;6. https://doi.org/10.3389/fnhum.2012.00189.
[26] Gallagher HL, Frith CD. Functional imaging of ‘theory of mind. Trends Cogn Sci
(Regul. Ed.) 2003;7(2):77–83. https://doi.org/10.1016/S1364-6613(02)00025-6.
[27] Henry JD, von Hippel W, Molenberghs P, Lee T, Sachdev PS. Clinical assessment of
social cognitive function in neurological disorders. Nature Rev Neurol 2016;12(1):
28–39. https://doi.org/10.1038/nrneurol.2015.229.
[28] Cotter J, Granger K, Backx R, Hobbs M, Looi CY, Barnett JH. Social cognitive
dysfunction as a clinical marker: a systematic review of meta-analyses across 30
clinical conditions. Neuroscience & Biobehavioral Reviews 2018;84:92–9. https://
doi.org/10.1016/j.neubiorev.2017.11.014.
[29] Broicher SD, 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(1):118–28. https://doi.org/
10.1016/j.neuropsychologia.2011.11.005.
[30] Realmuto S, Zummo L, Cerami C, Agrò L, Dodich A, Canessa N, Zizzo A, Fierro B,
Daniele O. Social cognition dysfunctions in patients with epilepsy: evidence from
patients with temporal lobe and idiopathic generalized epilepsies. Epilepsy Behavr
2015;47:98–103. https://doi.org/10.1016/j.yebeh.2015.04.048.
[31] Hennion S, Delbeuck X, Duhamel A, Lopes R, Semah F, Tyvaert L, Derambure P,
Szurhaj W. Characterization and prediction of theory of mind disorders in temporal
lobe epilepsy. Neuropsychology 2015;29(3):485–92. https://doi.org/10.1037/
neu0000126.
[32] Meletti S, Benuzzi F, Cantalupo G, Rubboli G, Tassinari CA, Nichelli P. Facial
emotion recognition impairment in chronic temporal lobe epilepsy. Epilepsia 2009;
50(6):1547–59. https://doi.org/10.1111/j.1528-1167.2008.01978.x.
73
Seizure: European Journal of Epilepsy 93 (2021) 63–74
[33] Edwards M, Stewart E, Palermo R, Lah S. Facial emotion perception in patients
with epilepsy: a systematic review with meta-analysis. Neuroscience &
Biobehavioral Reviews 2017;83:212–25. https://doi.org/10.1016/j.
neubiorev.2017.10.013.
[34] Monti G, Meletti S. Emotion recognition in temporal lobe epilepsy: a systematic
review. Neurosci Biobehavioral Rev 2015;55:280–93. https://doi.org/10.1016/j.
neubiorev.2015.05.009.
[35] Bonilha L, Nesland T, Martz GU, Joseph JE, Spampinato MV, Edwards JC,
Tabesh A. Medial temporal lobe epilepsy is associated with neuronal fibre loss and
paradoxical increase in structural connectivity of limbic structures. Journal of
Neurology, Neurosurgery & Psychiatry 2012;83(9):903–9. https://doi.org/
10.1136/jnnp-2012-302476.
[36] Steiger BK, Muller AM, Spirig E, Toller G, Jokeit H. Mesial temporal lobe epilepsy
diminishes functional connectivity during emotion perception. Epilepsy Res 2017;
134:33–40. https://doi.org/10.1016/j.eplepsyres.2017.05.004.
[37] Huang Y, Dupont P, Van de Vliet L, Jastorff J, Peeters R, Theys T, Loon J, Van
Paesschen W, Van den Stock J, Vandenbulcke M. Network level characteristics in
the emotion recognition network after unilateral temporal lobe surgery. Eur J
Neurosci 2020;52(5):3470–84. https://doi.org/10.1111/ejn.14849.
[38] Li Y-H, Chiu M-J, Yeh Z-T, Liou H-H, Cheng T-W, Hua M-S. Theory of Mind in
Patients with Temporal Lobe Epilepsy. J Int Neuropsychological Society 2013;19
(5):594–600. https://doi.org/10.1017/S1355617713000143.
[39] Giovagnoli AR, Franceschetti S, Reati F, Parente A, Maccagnano C, Villani F,
Spreafico R. Theory of mind in frontal and temporal lobe epilepsy: cognitive and
neural aspects: theory of Mind and Epilepsy. Epilepsia 2011;52(11):1995–2002.
https://doi.org/10.1111/j.1528-1167.2011.03215.x.
[40] Bala A, Okruszek Ł, Piejka A, Głębicka A, Szewczyk E, Bosak K, Szantroch M,
Hyniewska S, Rysz A, Marchel A. Social Perception in Mesial Temporal Lobe
Epilepsy: interpreting Social Information From Moving Shapes and Biological
Motion. J Neuropsychiatry Clin Neurosci 2018;30(3):228–35. https://doi.org/
10.1176/appi.neuropsych.17080153.
[41] Hennion S, Delbeuck X, Koelkebeck K, Brion M, Tyvaert L, Plomhause L,
Derambure P, Lopes R, Szurhaj W. A functional magnetic resonance imaging
investigation of theory of mind impairments in patients with temporal lobe
epilepsy. Neuropsychologia 2016;93:271–9. https://doi.org/10.1016/j.
neuropsychologia.2016.11.007.
[42] Laufs H, Hamandi K, Salek-Haddadi A, Kleinschmidt AK, Duncan JS, Lemieux L.
Temporal lobe interictal epileptic discharges affect cerebral activity in “default
mode” brain regions. Hum Brain Mapp 2006;28(10):1023–32. https://doi.org/
10.1002/hbm.20323.
[43] Ives-Deliperi VL, Jokeit H. Impaired Social Cognition in Epilepsy: a Review of What
We Have Learnt From Neuroimaging Studies. Front Neurol 2019;10:940. https://
doi.org/10.3389/fneur.2019.00940.
[44] Morou N, Papaliagkas V, Markouli E, Karagianni M, Nazlidou E, Spilioti M,
Afrantou T, Kimiskidis VK, Foroglou N, Kosmidis MH. Theory of Mind impairment
in focal versus generalized epilepsy. Epilepsy & Behav 2018;88:244–50. https://
doi.org/10.1016/j.yebeh.2018.09.026.
[45] Schacher M, Winkler R, Grunwald T, Kraemer G, Kurthen M, Reed V, Jokeit H.
Mesial Temporal Lobe Epilepsy Impairs Advanced Social Cognition. Epilepsia
2006;47(12):2141–6. https://doi.org/10.1111/j.1528-1167.2006.00857.x.
[46] Stewart E, Lah S, Smith ML. Patterns of impaired social cognition in children and
adolescents with epilepsy: the borders between different epilepsy phenotypes.
Epilepsy & Behav 2019;100:106146. https://doi.org/10.1016/j.
yebeh.2019.01.031.
[47] Guida M, Caciagli L, Cosottini M, Bonuccelli U, Fornai F, Giorgi FS. Social
cognition in idiopathic generalized epilepsies and potential neuroanatomical
correlates. Epilepsy & Behav 2019;100:106118. https://doi.org/10.1016/j.
yebeh.2019.01.003.
[48] Stewart E, Catroppa C, Lah S. Theory of Mind in Patients with Epilepsy: a
Systematic Review and Meta-analysis. Neuropsychol Rev 2016;26(1):3–24.
https://doi.org/10.1007/s11065-015-9313-x.
[49] Sherman EMS, Wiebe S, Fay-McClymont TB, Tellez-Zenteno J, Metcalfe A,
Hernandez-Ronquillo L, Hader WJ, Jetté N. Neuropsychological outcomes after
epilepsy surgery: systematic review and pooled estimates: cognitive Change after
Epilepsy Surgery. Epilepsia 2011;52(5):857–69. https://doi.org/10.1111/j.1528-
1167.2011.03022.x.
[50] 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):194–8. https://doi.org/10.1016/j.yebeh.2012.04.115.
[51] Rice GE, Hoffman P, Lambon Ralph MA. Graded specialization within and between
the anterior temporal lobes. Ann N Y Acad Sci 2015;1359(1):84–97. https://doi.
org/10.1111/nyas.12951.
[52] Olson IR, McCoy D, Klobusicky E, Ross LA. Social cognition and the anterior
temporal lobes: a review and theoretical framework. Soc Cogn Affect Neurosci
2013;8(2):123–33. https://doi.org/10.1093/scan/nss119.
[53] Kirsch HE. Social cognition and epilepsy surgery. Epilepsy & Behav 2006;8(1):
71–80. https://doi.org/10.1016/j.yebeh.2005.09.002.
[54] Wilson SJ, Bladin PF, Saling MM. The burden of normality: a framework for
rehabilitation after epilepsy surgery: rehabilitation after Epilepsy Surgery.
Epilepsia 2007;48:13–6. https://doi.org/10.1111/j.1528-1167.2007.01393.x.
[55] Shaw P, Lawrence E, Bramham J, Brierley B, Radbourne C, David AS. A prospective
study of the effects of anterior temporal lobectomy on emotion recognition and
theory of mind. Neuropsychologia 2007;45(12):2783–90. https://doi.org/
10.1016/j.neuropsychologia.2007.04.020.
[56] Amlerova J, Cavanna AE, Bradac O, Javurkova A, Raudenska J, Marusic P. Emotion
recognition and social cognition in temporal lobe epilepsy and the effect of
B. Mikula et al.
epilepsy surgery. Epilepsy & Behav 2014;36:86–9. https://doi.org/10.1016/j.
yebeh.2014.05.001.
[57] Cohn M, St-Laurent M, Barnett A, McAndrews MP. Social inference deficits in
temporal lobe epilepsy and lobectomy: risk factors and neural substrates. Soc Cogn
Affect Neurosci 2015;10(5):636–44. https://doi.org/10.1093/scan/nsu101.
[58] 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(2–3):150–7. https://doi.org/10.1016/j.eplepsyres.2008.03.018.
[59] 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(1):12–6. https://
doi.org/10.1016/j.yebeh.2013.03.022.
[60] Ammerlaan E, Hendriks PH, Colon AJ, Kessels RPC. Emotion perception and
interpersonal behavior in epilepsy patients after unilateral amygdalohip-
pocampectomy. Acta Neurobiol. Exp. 2008;68:214–8.
[61] Anderson AK, Spencer DD, Fulbright RK, Phelps EA. Contribution of the
anteromedial temporal lobes to the evaluation of facial emotion. Neuropsychology
2000;14(4):526.
[62] Gosselin N, Peretz I, Noulhiane M, Hasboun D, Beckett C, Baulac M, Samson S.
Impaired recognition of scary music following unilateral temporal lobe excision.
Brain 2005;128(3):628–40. https://doi.org/10.1093/brain/awh420.
[63] McClelland S, Garcia RE, Peraza DM, Shih TT, Hirsch LJ, Hirsch J, Goodman RR.
Facial Emotion Recognition after Curative Nondominant Temporal Lobectomy in
Patients with Mesial Temporal Sclerosis. Epilepsia 2006;47(8):1337–42. https://
doi.org/10.1111/j.1528-1167.2006.00557.x.
[64] Meletti S, Picardi A, De Risi M, Monti G, Esposito V, Grammaldo LG, Di Gennaro G.
The affective value of faces in patients achieving long-term seizure freedom after
temporal lobectomy. Epilepsy & Behav 2014;36:97–101. https://doi.org/10.1016/
j.yebeh.2014.05.002.
[65] Van de Vliet L, Jastorff J, Huang Y-A, Van Paesschen W, Vandenbulcke M, Van den
Stock J. Anterior Temporal Lobectomy Impairs Neural Classification of Body
Emotions in Right Superior Temporal Sulcus and Reduces Emotional Enhancement
in Distributed Brain Areas without Affecting Behavioral Classification. The J
Neurosci 2018;38(43):9263–74. https://doi.org/10.1523/JNEUROSCI.0634-
18.2018.
[66] Wendling A-S, Steinhoff BJ, Bodin F, Staack AM, Zentner J, Scholly J, Valenti M-P,
Schulze-Bonhage A, Hirsch E. Selective amygdalohippocampectomy versus
standard temporal lobectomy in patients with mesiotemporal lobe epilepsy and
74
Seizure: European Journal of Epilepsy 93 (2021) 63–74
unilateral hippocampal sclerosis: post-operative facial emotion recognition
abilities. Epilepsy Res 2015;111:26–32. https://doi.org/10.1016/j.
eplepsyres.2015.01.002.
[67] Benuzzi F, Zamboni G, Meletti S, Serafini M, Lui F, Baraldi P, Duzzi D, Rubboli G,
Tassinari CA, Nichelli PF. Recovery from Emotion Recognition Impairment after
Temporal Lobectomy. Front Neurol 2014;5. https://doi.org/10.3389/
fneur.2014.00092.
[68] Giovagnoli AR, Parente A, Didato G, Deleo F, Villani F. Expanding the spectrum of
cognitive outcomes after temporal lobe epilepsy surgery: a prospective study of
theory of mind. Epilepsia 2016;57(6):920–30. https://doi.org/10.1111/epi.13384.
[69] Kumfor F, Honan C, McDonald S, Hazelton JL, Hodges JR, Piguet O. Assessing the
“social brain” in dementia: applying TASIT-S. Cortex 2017;93:166–77. https://doi.
org/10.1016/j.cortex.2017.05.022.
[70] Genova HM, McDonald S. Social Cognition in Individuals with Progressive Multiple
Sclerosis: a Pilot Study Using TASIT-S. J Int Neuropsychol Society 2020;26(5):
539–44. https://doi.org/10.1017/S1355617719001371.
[71] Baxendale S, Wilson SJ, Baker GA, Barr W, Helmstaedter C, Hermann BP,
Langfitt J, Reuner G, Rzezak P, Samson S, Smith M-L. Indications and expectations
for neuropsychological assessment in epilepsy surgery in children and adults.
Epileptic Disorders 2019;21(3):221–34. https://doi.org/10.1684/epd.2019.1065.
[72] Giovagnoli AR, Parente A, Villani F, Franceschetti S, Spreafico R. Theory of mind
and epilepsy: what clinical implications? Epilepsia 2013;54(9):1639–46. https://
doi.org/10.1111/epi.12255.
[73] Wang W-H, Shih Y-H, Yu H-Y, Yen D-J, Lin Y-Y, Kwan S-Y, Chen C, Hua M-S.
Theory of mind and social functioning in patients with temporal lobe epilepsy.
Epilepsia 2015;56(7):1117–23. https://doi.org/10.1111/epi.13023.
[74] Altman DG, Royston P. The cost of dichotomising continuous variables. BMJ 2006;
332(7549):1080. https://doi.org/10.1136/bmj.332.7549.1080. 1.
[75] Isik L, Koldewyn K, Beeler D, Kanwisher N. Perceiving social interactions in the
posterior superior temporal sulcus. Proceedings of the Nat Academy of Sci 2017;
114(43):E9145–52. https://doi.org/10.1073/pnas.1714471114.
[76] Helmstaedter C, Elger CE, Vogt VL. Cognitive outcomes more than 5 years after
temporal lobe epilepsy surgery: remarkable functional recovery when seizures are
controlled. Seizure 2018;62:116–23. https://doi.org/10.1016/j.
seizure.2018.09.023.
[77] Mazur-Mosiewicz A, Carlson HL, Hartwick C, Dykeman J, Lenders T, Brooks BL,
Wiebe S. Effectiveness of cognitive rehabilitation following epilepsy surgery:
current state of knowledge. Epilepsia 2015;56(5):735–44. https://doi.org/
10.1111/epi.12963.