Neurocase, 2013

http://dx.doi.org/10.1080/13554794.2013.826695

Emergence of hyper empathy after right

amygdalohippocampectomy

Aurélie Richard-Mornas1 , Audric Mazzietti2 , Olivier Koenig2 , Céline Borg1 ,

Philippe Convers1 , and Catherine Thomas-Antérion1,2
1
Unit of Neuropsychology-CM2R, Department of Neurology, CHU Nord, Saint-Etienne, France
2
Laboratory for the Study of Cognitive Mechanisms, University Lyon 2, Lyon, France
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We report a fascinating case of a patient with a hyper empathy that appeared after resective epilepsy surgery.
This behavioral modification has remained unchanged since the surgery took place 13 years ago. Recent
neuropsychological objective assessments confirmed hyper empathy in a self-report questionnaire, and revealed
higher affective theory of mind than controls in a “Reading the Mind in the Eyes Task.” Temporal lobe epilepsy
is the most common form of epilepsy and the investigation of emotional processes after surgery in these patients
deserves to be related.

Keywords: Temporal lobe epilepsy surgery; Behavioral neurology; Neuropsychology; Empathy; Affective theory of
mind.

Psychopathology is prevalent in patients with com-
plex partial seizures and temporal focus (tempo-
ral lobe epilepsy, TLE), especially when they suf-
fer from severe, medically drug-resistant epilepsy,
and temporal seizures. Psychiatric disorders consti-
tute a large part of the illness burden of patients
with epilepsy, both before and after anterior tem-
poral lobectomy. They are major determinants
of patients’ self-perceived quality of life, and are
thought to play a major part in outcome after resec-
tive epilepsy surgery (Cankurtaran, Ulug, Saygi,
Tiryaki, & Akalan, 2005). After anterior temporal
lobectomy, new psychiatric disorders can be fre-
quently observed, peculiarly mood disorders, such
as major depression, dysthymia, and anxiety disor-
ders (Glosser, Zwil, Glosser, O’Connor, & Sperling,
2000). Recently, different studies have focused on
the investigation of emotional and social compe-
tence in patients with TLE (Meletti, Benuzzi, &
Rubboli, 2003; Shaw et al., 2007). The authors
evaluated recognition of facial expressions and
advanced social cognition abilities, above all cog-
nitive theory of mind. Impairment predominated
for the processing of negative facial expressions
in patients after right temporal lobectomy, as well
as in patients with medically drug-resistant epilep-
tic seizures before surgery (Adolphs, Tranel, &
Damasio, 2001).
Theory of mind is the ability to infer peo-
ple’s mental states (Premack & Woodruff, 1978).
It allows individuals both to ascribe cognitive
and affective states to others and to deduce their
intentions from their attitudes (Coricelli, 2005).
A distinction can be made between cognitive the-
ory of mind, which concerns the cognitive states,
beliefs, or intentions of other people (Coricelli,
2005), and affective theory of mind, which con-
cerns the affective states, emotions, or feelings
of others. Although some researchers hold that
affective theory of mind is similar to empathy

Address correspondence to Aurélie Richard-Mornas, Unit of Neuropsychology-CM2R, Department of Neurology, CHU Nord,
42055 Saint-Etienne cx 02, France. (E-mail: aurel.richard@gmail.com
No conflicts of interest.

c 2013 Taylor & Francis

⃝
 2 RICHARD-MORNAS ET AL.
(Decety & Lamm, 2006), these two concepts are
actually somewhat different. While both conduct to
the real understanding of mental affective states,
we consider that the term empathy refers to the
feeling and experiencing of another person’s emo-
tion, whereas affective theory of mind refers to the
ability to adopt the other person’s point of view,
or “put oneself in his/her shoes,” without neces-
sarily experiencing any emotion (Pacherie, 2004).
Shamay-Tsoory (2011) describes two separate sys-
tems for empathy: the “emotional empathy” sys-
tem described above and the “cognitive empathy”
system, which is synonymous with affective the-
ory of mind. In the present paper, we report a
fascinating case of a patient with a hyper empa-
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thy associated with exceptional performance in
a task of affective theory of mind after right
amygdalohippocampectomy.
METHODS
A 37-year-old, right-handed woman experienced
the onset of seizures at the age of 2 years. Her initial
symptoms were eye staring, pallor, verbal, and swal-
lowing automatisms with loss of contact without
secondary generalization. The scalp EEG revealed
a definitive electrical correlate for right TLE. Until
17 years old, she was under barbiturate treatment
at low doses and seizures resolved. Then, her TLE
Figure 1. A magnetic resonance imaging of the patient after surgery: right mesial temporal lobectomy including amygdala and
hippocampal region and regions of the lateral temporal lobe.
became more severe with multiple daily seizures,
despite the association of three anti-epileptic drugs.
Cerebral MRI showed cortical dysplasia in the right
inferior temporal lobe. The patient underwent right
mesial temporal lobectomy including amygdala and
hippocampal region, and regions of the lateral tem-
poral lobe that were involved in the lesional process.
Figure 1 shows a magnetic resonance imaging of the
patient after surgery. The pathology demonstrated
cortical dysplasia. The patient was seizure free after
the surgical intervention. She was followed-up for
13 years at the hospital and has been monitored
closely since the operation. A few weeks after the
lobectomy, she told about the emergence of hyper
empathy. She began to feel physical effects when
experiencing emotions, especially sadness (“spin
at the heart”) and anger (“esophageal unpleasant
feeling”) when meeting with relatives or strangers,
seeing a person on TV, or reading about a char-
acter in a novel. These effects were automatic and
irrepressible, and referred to her emotional empa-
thy. Moreover, she described an increased ability to
decode others’ mental states, including their emo-
tions, without necessarily experiencing any emotion
(it refers to her affective theory of mind). Her family
confirmed this new impulsive empathy. This phe-
nomenon remained unchanged for 13 years. Since
surgery, she got married, had a child, and had a
full-time job. She has a successful family and social
life.
 HYPER EMPATHY AFTER AMYGDALOHIPPOCAMPECTOMY
We evaluated this unusual behavioral modifica-
tion with a battery of neuropsychological tests.
Our clinical research protocol was agreed by the
French local ethics review board (Institutional
Review Board Information IORG0004981). First of
all, a neuropsychological test battery was adminis-
tered that included the Verbal and Performance IQ
(WAIS-R), the Free and Cued Selective Reminding
Test (FCSRT) for verbal episodic memory, the
Battery of Memory Efficiency (BEM) for visual
memory, the Trail Making test (TMT part A and
B) for executive functions, verbal fluency tests,
and the WAIS-R Block design test for visuospatial
abilities.
Moreover, we performed a psychiatric diagno-
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sis, based on the criteria of the Diagnostic and
Statistical Manual of Mental Disorders, Fourth
Edition (DSM-IV). The Beck Depression Inventory
version II (BDI-II) was used to evaluate depres-
sion. The State Trait Inventory Anxiety (STAI)
was administered to rate the severity of anxiety
and, the Yale-Brown obsessive compulsive scale
(Y-BOCS) was used to rate obsessive compulsive
disorders. We also used the Rorschach test to eval-
uate the patient’s personality features. In addition
to the mood disorders and personality evaluation
tests, we administered the Empathy Quotient (EQ),
(Lawrence, Shaw, Baker, Baron-Cohen, & David,
2004) a self-report questionnaire made of 40 empa-
thy and 20 control items. Among the empathy items
we analyzed three factors. The first factor, “cogni-
tive empathy,” which is synonymous with affective
theory of mind, includes items that measure the
appreciation of affective states (e.g., “I am good at
predicting how someone will feel”). The second fac-
tor, “emotional reactivity,” which is synonymous
with emotional empathy, reflects the tendency to
have an emotional reaction in response to others’
mental states (e.g., “I get upset if I see people suf-
fering on news programmes”). And the third factor
is “social skills.” Then, we assessed the affective the-
ory of mind using a French version of the Reading
the Mind in the Eyes Test (Lawrence et al., 2004).
It consisted of 36 black-and-white photographs of
the eye region of actors who were asked to pro-
duce different facial expressions. Under each pic-
ture, four adjectives (one target and three foils)
described basic or complex emotions and the task
consisted of selecting the adjective that described
at best the person’s mental state. This measures
peoples’ ability to decipher a mental state from pic-
tures of the eyes alone, which is, according to the
authors, an advanced measure of mind-reading or,
3
in our terminology, a measure of the affective the-
ory of mind. This task was proposed to the patient
and to 10 healthy French control women (mean age
= 39, SD = 3.19 years), with no prior history of
any neurological and psychiatric illness. Testing a
control group was necessary, because there are no
French norms of the Eyes Test. Finally, we admin-
istered the TOM-15 that is to say a false-belief task
to assess cognitive theory of mind. It refers to the
ability to deduce the mental states of other peo-
ple, such as their beliefs and intentions (Desgranges
et al., 2012). It consisted of 15 stories (8 of 1st
order and 7 of 2nd order). The stories described
everyday situations that give rise to a mistaken
belief about the actual state of the world in one of
the characters. Most of these stories are original,
and some inspired by literature (“ally and Ann”,
Baron-Cohen, Leslie, & Frith, 1985).
RESULTS
The traditional assessment of cognitive functions
was normal (normal scales in FCSRT, BEM, TMT
A and B, verbal fluency, and Block design). The
Verbal and Performance IQ scores were 93 and 93,
respectively. The patient was neither depressed (nor-
mal scale in BDI-II, score = 13, range: 8–15) nor
anxious (normal scales in STAI-state, score = 50,
range: 46–55 and STAI-trait, score = 65, range
56–65). The patient score was in the sub-clinical
range in Y-BOCS (score = 7, range 0–7). The
Rorschach test confirmed that the patient did not
have personality disorder nor psychotic or neurotic
or borderline disorders. The patient is grounded in
reality with a normal considered good form score
(F+ %). This was confirmed with a normal num-
ber of responses called banalities. In the EQ, her
performance was above average (score = 55, range:
33–52). The patient scored high in the subscale
“emotional reactivity” (score = 17/24) and in the
factor “cognitive empathy” (score 26/26). Finally,
the French version of the Eyes Test allowed us to
assess the affective theory of mind of the patient.
Scores were analyzed with a Crawford and Howell
(1998) t-test for singles-cases. This analysis revealed
that the patient scored significantly higher than
controls (patient score = 26; mean controls score
= 21, SD = 1.9), p < .0001. This result is illus-
trated in Figure 2. In the TOM-15, her performance
was normal (score = 14, mean controls score =
14.06, SD = 0.96). Neuropsychological objective
assessments thus confirmed the emergence of hyper
 4 RICHARD-MORNAS ET AL.
Figure 2. Patient’s number of correct choices (max = 36) and
mean score of normal controls on the Eyes Test (chance = 9).
∗ Denotes p < .0001.
emotional empathy and affective theory of mind
(cognitive empathy) with higher scores than con-
trols. However, her cognitive theory of mind was
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not affected by the resection.
DISCUSSION
We showed impulsive empathy in a self-report ques-
tionnaire and we evidenced higher affective theory
of mind than controls (which concerns the affective
states, emotions, or feelings of others) in a patient
who reported a new spectacular emotional arousal,
after right amygdalohippocampectomy. We con-
firmed normal performance in a cognitive theory of
mind test, i.e., the ability to deduce the mental states
of other people, as their beliefs and intentions.
One model for describing how people infer the
intentions of others from their actions is the system
represented by the “mirror neurons” (Rizzolatti,
Fadiga, Gallese, & Fogassi, 1996). Mirror neu-
rons have been discovered in the inferior frontal
cortex of monkeys (inferior premotor area F5).
These cells are active when the monkey makes a
goal-oriented movement (e.g., grasping food) and
when the monkey observes the experimenter or
another monkey executing the same movement (di
Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti,
1992). The existence of mirror neurons indicates
the ability of the brain to replicate and mimic the
action, emotion, and intention of the other person.
This concept leads to a comprehension of theory
of mind, i.e., the ability to adopt the other per-
son’s point of view, or to “put oneself in his/her
shoes.”
Our observations are consistent with the ones
from other authors (Shamay-Tsoory, 2011) who
describe two separate systems for empathy: the
“emotional empathy” and the “cognitive empathy”
system, which is synonymous with affective theory
of mind. Cognitive empathy, defined as the ability
to “step into the shoes of another person to under-
stand his feelings,” is based on a neural network
that is not yet fully understood. This affective the-
ory of mind-related cerebral network seems to be
constituted by the right prefrontal cortex, includ-
ing the orbital and medial prefrontal cortices, the
right temporal lobe and the amygdala (Carrington
& Bailey, 2009). There is imaging and clinical
(Baron-Cohen et al., 1999) evidence that shows that
the amygdala region represents an important input
for the mind-reading system. Especially, the imag-
ing study (fMRI) by Baron-Cohen et al. (1999)
showed amygdala activation in normal subjects
inferring complex mental states from images of the
eyes when performing the “Reading the Mind in the
Eyes Task.” Moreover, studies (see, e.g., Carrington
& Bailey, 2009) suggest that the contribution of the
right prefrontal cortex in social attribution and in
theory of mind tasks allows the subject to divest
from his own point of view and better understand
others’ mental states. The present case report sug-
gests that a new permanent cortical organization of
attention and emotion processes has developed in
our patient that may be responsible for an enhance-
ment of affective theory of mind. This cerebral
network may involve the right prefrontal cortex and
the amygdala. This paper provides a novel frame-
work on the investigation of emotional competence
in patients with TLE.
Original manuscript received 2 February 2013
Revised manuscript received 12 June 2013
First published online 16 August 2013
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