Epilepsy & Behavior 19 (2010) 643–646

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Epilepsy & Behavior

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / ye b e h

Case Report

Long-term neuropsychological follow-up of a child with Klüver–Bucy syndrome

Morris J. Cohen a,⁎, Yong D. Park a, Hyunmi Kim a,1, Jay J. Pillai b,2
a
Department of Neurology, Medical College of Georgia, Augusta, GA, USA
b
Department of Neuroradiology, Medical College of Georgia, Augusta, GA, USA

a r t i c l e i n f o a b s t r a c t

Article history: We describe the case of a 10-year-old girl who developed behavioral changes consistent with Klüver–Bucy
Received 1 September 2010 Syndrome following Listeria meningoencephalitis at 2½ years of age. MRI at age 4 revealed evidence of diffuse
Accepted 7 September 2010 brain atrophy with predominant temporal lobe involvement. Electroencephalograpy at 9½ years of age
showed abnormal electrical discharges from the left temporal area. Follow-up MRI with volumetric analysis of
Keywords: the mesial temporal structures at 9 years of age demonstrated decreased hippocampal volume bilaterally.
Kluver–Bucy syndrome
Consistent with the morphological abnormalities, serial neuropsychological evaluations demonstrated
Neuropsychological follow-up
Child
expressive and receptive language impairment and an amnestic syndrome that significantly decreased her
ability to make new declarative memories and maintain adequate academic progress.
© 2010 Elsevier Inc. All rights reserved.

1. Introduction behavioral changes has been recognized as the “complete syndrome,”

Klüver–Bucy Syndrome (KBS) is a rare constellation of neurobe-
havioral signs and symptoms following bilateral insult to the mesial
temporal lobes. It was first described in rhesus monkeys by Heinrich
Klüver and Paul Bucy following large resections of the temporal lobes
[1–3]. Classically, these animals lacked the ability to recognize objects
visually (they could not distinguish edible from inedible objects), had
a striking tendency to examine objects orally, were unusually alert
and responsive to visual stimuli (they touched or mouthed every
object in their visual field), were rather placid, became hypersexual,
and increased their food intake. The authors termed this group of
symptoms temporal lobe syndrome.
The first case of KBS in humans was described by Terzian and Dalle
Ore [4] in 1955 following bilateral temporal lobectomy for intractable
epilepsy and was also described later following viral meningoenceph-
alitis [5]. In adults, the characteristic features of KBS include: visual
agnosia, the inability to recognize objects without the loss of visual
discrimination; hyperorality, a strong urge to examine all objects with
the mouth; hypermetamorphosis, excessive attentiveness/touching of
visual stimuli; placidity, loss of the normal fear or anger response;
indiscriminant hypersexuality; and changes in dietary habits [4,5].
Other less commonly reported features of KBS in humans include
aphasia, memory disturbance, and seizures [6,7]. This constellation of
⁎ Corresponding author. Medical College of Georgia, 1120 15th Street, Bt-2601,
Augusta, GA 30912, USA. Fax: + 1 706 721 5238.
E-mail address: mcohen@mail.mcg.edu (M.J. Cohen).
1
Current address: University of Alabama, 1600 6th Ave S, Children's Harbor Building,
Suite 314, Birmingham, AL 35233, USA.
2
Current address: Department of Radiology, Johns Hopkins University, 600 North
Wolfe Street, B100-G Phipps Building, Baltimore, MD 21287, USA.
although in humans it is more common to observe the “incomplete
syndrome,” which typically comprises at least three key components of
the full syndrome [6,8].
This syndrome is rare in adults and even less common in children.
Excluding the current report, 26 pediatric cases have previously been
published in the literature. To date, two pediatric series have been
published reporting 13 children and adolescents with KBS ranging in
age from 2½ to 14 [9,10]. Of these patients, 8 had herpes simplex
encephalitis, 2 had anoxic–ischemic encephalopathy, and the remaining
cases had traumatic brain injury, tuberous meningitis, and neurocysti-
cercosis. Additional single case studies of pediatric KBS have been
reported in association with heat stroke [11], methotrexate leukoence-
phalopathy [12], mycoplasmal bronchitis [13], bilateral temporal
congenital malformations [14], bilateral arachnoid cysts [15], Reye
syndrome [16], shigellosis [17], and unidentified encephalopathic
illness [18].
None of these pediatric clinical presentations involved the “complete
syndrome.” On the basis of detailed review of the information provided
in the 26 previously reported pediatric KBS cases, hyperorality and
hypersexuality were the most common features, as these were reported
in 88% (23/26) of the cases, followed by bulimia (65%, 17/26). Visual
agnosia, hypermetamorphosis, and placidity occurred in approximately
50% of the patients. Furthermore, seizures and emotional/behavioral
disturbances were each reported in 69% (18/26) of the cases.
In contrast, the incidence and severity of language and memory
impairment were difficult to quantify because of the lack of detailed
neuropsychological evaluation and follow-up. In the majority of cases,
the absence of formal assessment was the result of poor testing
compliance on the part of the patient at the time of diagnosis/treatment
or loss of the child/adolescent to follow-up when the evaluation could
be conducted in a valid manner.

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644 M.J. Cohen et al. / Epilepsy & Behavior 19 (2010) 643–646

Three of the reports included the results of intellectual assessment.
The first case [14] was an 11-year-old boy with global impairment on
the Wechsler Intelligence Scale for Children, Third Edition (WISC-III
Full Scale IQ [FSIQ] = 58). The second case [18] was a 13-year-old boy
whose WISC Verbal IQ improved from “low average” (score not
reported) to average (VIQ = 107) and his Performance IQ improved
from “mildly deficient” to low average (PIQ = 90) 8 months after
diagnosis/treatment. In the third case [15], the 11-year-old boy's
WISC-R VIQ was deficient (VIQ = 54), which was contrasted sharply
by his low average PIQ (PIQ = 87). In addition, formal language
assessment revealed “an overall delay in receptive and expressive
language.” On the basis of a review of 13 cases reporting results from
mental status examinations, evidence supporting language impairment
was evident in 6 additional cases (7 total, 54%) and difficulty with
“short-term memory” was present in 8 (62%) of those same cases.
We present the first report documenting the long-term cognitive
and behavioral outcome (7½ years postonset) in a young girl with
behavioral changes consistent with Klüver–Bucy syndrome (“incom-
plete syndrome”) following Listeria meningoencephalitis.
2. Case report
This 10-year-old right-handed girl contracted Listeria monocyto-
genes meningoencephalitis at 2½ years of age. Prior to this event, the
pregnancy, vaginal delivery, and developmental progression for both
motor and language milestones were all normal. Initially, the patient
was transferred from a local hospital where she was being treated for
dehydration following a week of fever, vomiting, diarrhea, and
abdominal pain. On the night of admission, she developed generalized
status epilepticus lasting 45 minutes, which was initially treated with
phenytoin and subsequently changed to carbamazepine. A ventricu-
loperitoneal shunt was placed because of postinfectious communi-
cating hydrocephalus. The child was discharged on carbamazepine.
She remained seizure free, and carbamazepine was discontinued at
3 years 10 months of age.
Two months after discharge, she began exhibiting significant
behavioral change characterized by aggression toward family members
and pets, uncontrolled screaming and crying, difficulty focusing and
sustaining her attention span, hyperactivity, and decreased language
output along with mild stuttering. These behavior problems persisted,
and at 4½ she began exhibiting hypersexuality (frequent masturbation),
hyperorality, and significant weight gain (25 pounds at 2.5 years;
87 pounds at 5.5 years). The behavioral problems were initially treated
with clonidine; methylphenidate (Concerta) was subsequently added to
improve attention span and decrease hyperactivity.
Initial neuropsychological evaluation was performed at 5½ years of
age. At this time, she was attending a 4-year kindergarten program
and receiving speech/language therapy through the special education
program at her school. Following this evaluation, preschool special
education classroom services including accommodations and a
behavior management program were added to the individual
educational program (IEP). Follow-up neuropsychological evaluations
were conducted at 7 (first grade) and 10 (third grade) years of age,
and modifications to the child's special education IEP were made
following each evaluation.
At 6 years of age, she developed complex partial seizures
characterized by episodes of gibberish and decreased responsiveness.
The seizures were successfully controlled with extended-release
capsule carbamazepine; however, once she reached 9½ years of age,
her seizures resumed and lamotrigine was added, resulting in
decreased seizure frequency (from 15–20 to 1–5 seizures/month).
2.1. Neurological findings
During neurological examinations over the past 7 years, the child
typically presented as cooperative and pleasant; however, she
exhibited a tendency to cling to the examiner with tactile exploratory
behavior. She smiled spontaneously and her speech was fluent, but
she did not initiate conversation during the examinations. Cranial
nerves II through XII were intact. Motor function was measured 5/5
for power, with normal bulk and tone. Reflexes and gait were normal.
Romberg and tandem gait were also normal.
2.2. EEG monitoring
An EEG obtained following the onset of the complex partial seizures
when she was 6 years old showed focal slowing bilaterally (RN L), with
epileptiform discharges present over the right midtemporal region. A

Fig. 1. (A) FLAIR sequence of axial view revealed bilateral increased signal over both hippocampi. (B) The hippocampal volumes were computed by summation of volumes on
consecutive coronal MPRAGE images. Imaging parameters for this sequence were: TR/TE/TI 11/4/400, flip angle 12, matrix 256 × 256, 1 NEX. These images were then reformatted in
the oblique coronal plane with 3.0-mm slice thickness such that the plane of reformatting was perpendicular to the longitudinal axis of each hippocampus. On each of these
reformatted coronal images, an ovoid region of interest was manually traced around each hippocampus or amygdala, and each hippocampal volume was computed as the sum of the
products of the region of interest area and effective slice thickness.
 M.J. Cohen et al. / Epilepsy & Behavior 19 (2010) 643–646 645

repeat EEG following the return of seizures at 9½ indicated bitemporal Table 1

slowing with epileptiform discharges from the left midtemporal region. Results of serial neuropsychological evaluations.

Domain 5 years 7 years 10 years

7 months 1 month 1 month

2.3. Neuroimaging Standard score

a
Intelligence DAS WISC-III/IV
Magnetic resonance imaging of the brain at 4 years of age revealed Verbal Cluster (DAS)
Verbal Comprehension Index (WISC) 73 77 63
diffuse brain atrophy with predominant bilateral temporal lobe
Nonverbal Cluster (DAS) 54 71 77
involvement. MRI at 9½ years of age showed increased signal over Perceptual Reasoning Index (WISC)
both hippocampi by FLAIR (Fig. 1A). Formal volumetric analysis of the Working Memory Index — 67 80
hippocampus and amygdala was performed on consecutive oblique Processing Speed Index — 64 75
General Cognitive Index (DAS) 63 69 68
coronal reformatted MPRAGE images (Fig. 1B), which were obtained
Full Scale IQ (WISC)
on a 1.5-T Siemens Vision MRI scanner (Erlangen, Germany). The Executive Functioning
summated volumes are as follows: right hippocampus, 1.230 cm3; left Tower (NEPSY) 70 65 65
hippocampus, 1.050 cm3; right amygdala, 1.2357 cm3; left amygdala, Receptive Language
1.3056 cm3. These findings revealed decreased volume of both the Phonological Processing (NEPSY) 110 80 75
Vocabulary (PPVT-III/IV) 84 80 64
right and left hippocampi compared with the normal value of
Sentence Repetition (NEPSY) 85 80 64
approximately 2.5 cm3 for this patient's age group [19]. Comprehension of Instructions (NEPSY) 95 80 80
Expressive Language
Picture Naming (EOWPVT) 65 71 60
Verbal Fluency (NEPSY) 80 70 85
2.4. Neuropsychological findings Vocabulary (WISC-III/IV) — 80 70
Visual–Spatial Perception
Gestalt Closure (KABC-II) 80 85 60
To monitor higher cortical functioning and make recommendations
Arrows (NEPSY) 95 80 65
regarding school placement and the need for additional therapeutic Visual–Motor Integration
interventions, detailed neuropsychological evaluation was performed at DTVMI 83 82 75
5, 7, and 10 years of age. Table 1 summarizes the results (standard scores Pattern Construction (DAS)
with a mean of 100 and SD of 15) of these evaluations, which cover the Block Design (WISC-III/IV) 95 80 65
Learning/Memory (Children's Memory Scale)
domains of Intelligence, Executive Functioning, Language, Visual– Working Memory
Spatial Perception, Visual–Motor Integration/Construction, Learning Numbers 75 80 75
and Memory, and Academic Achievement. Sequences 100 70 75
Review of these results indicates that the child consistently Picture Locations 80 80 55
Verbal Memory
performed in the mildly deficient to borderline range of intellectual
Stories Immediate 85 75 55
ability as measured by the General Conceptual Ability score (GCA) from Stories Delayed 75 65 55
the Differential Ability Scales (DAS) at 5½ and the Full Scale IQ score Word Pairs Immediate 65 55 55
(FSIQ) from the Wechsler Intelligence Scale for Children, Third/Fourth Word Pairs Delayed 60 60 55
Editions (WISC-III/IV), administered at 7 and 10 years of age. However, a Visual Memory
Dot Locations Immediate 90 65 80
significant decline in verbal conceptual ability (14 points on the Verbal
Dot Locations Delayed 85 85 85
Comprehension Index) was noted between the second and third Faces Immediate 85 75 70
evaluations. Higher-order sequential reasoning and problem-solving Faces Delayed 80 85 85
capability as measured with the Tower subtest of NEPSY (a pediatric Achievement
WRAT-3
version of the Tower of London) remained deficient to borderline,
Reading 91 79 72
consistent with intellectual expectancy. Linguistic functioning was Spelling 88 92 70
generally in the borderline to low average range, with a performance Arithmetic 97 65 69
decline noted on measures of both receptive and expressive language at GORT-4
10 years of age. Specifically, the child exhibited declines in her receptive Reading Fluency — — 55
Reading Comprehension — — 60
vocabulary development (PPVT-III), her ability to repeat sentences of
TOWL-3
increasing length, and her ability to comprehend multipart directions Written Expression — — 68
(NEPSY). She continued to demonstrate difficulty naming pictures to a
DAS, Differential Ability Scales; WISC-IV, Wechsler Intelligence Scale for Children,
confrontation (EOWPVT) and defining words (WISC-III/IV). The child Fourth Edition; PPVT, Peabody Picture Vocabulary Test; EOWPVT, Expressive One Word
demonstrated a similar pattern of performance when visual–spatial/ Picture Vocabulary Test; KABC, Kaufman Assessment Battery for Children; DTVM I,
constructional functioning was assessed. At age 10 she exhibited Developmental Test of Visual Motor Integration; WRAT, Wide Range Achievement Test;
declines in visual closure (KABC–II), her ability to judge spatial GORT, Gray Oral Reading Test; TOWL, Test of Written Language.

orientation (NEPSY), and her ability to construct geometric designs

with blocks (WISC-III/IV) as well as with paper and pencil (DTVMI).
Assessment of learning and memory (Children's Memory Scale)
revealed historically poor working memory and verbal learning curves
(Word Pairs Immediate). Further, delayed recall (30 minutes later) was
better preserved (borderline to low average) for visual as opposed to
verbal material, with a significant decline in verbal memory noted at age
10. Consistent with serial memory assessment, the results of academic
assessment indicated that the child's performance in the areas of
reading (letter/word recognition), spelling, and arithmetic decreased
from the low average/average range (standard scores = 88–97) at age 5
to the borderline range (standard scores = 69–72) at age 10. Further-
more, oral reading fluency, reading comprehension, and written
expression were all in the deficient range (standard scores = 55–68)
at age 10.
3. Discussion
Klüver–Bucy syndrome typically presents as a rare constellation of
behavioral symptoms resulting almost exclusively from bilateral
temporal lobe damage. Although rare in adults, this syndrome is
even less common in children. Further, in children, as is most often the
case in adults, the syndrome is frequently incomplete in that not all of
the typical neurobehavioral features of the syndrome are present.
646 M.J. Cohen et al. / Epilepsy & Behavior 19 (2010) 643–646
Consistent with the 26 previously reported pediatric cases, our
patient exhibited emotional/behavioral changes characterized by
aggression toward people and pets, uncontrolled screaming and
crying, social disinhibition, difficulty focusing/sustaining attention,
and hyperactivity. She also demonstrated hyperorality, altered dietary
habits with associated weight gain, and hypersexuality expressed as
frequent masturbation. In addition, our patient subsequently devel-
oped a seizure disorder, which occurred in 69% of the 26 pediatric
cases previously reported.
Serial neuropsychological assessment revealed bilateral higher
cortical dysfunction, with a significant cognitive decline noted in left
hemisphere functioning when the patient was seen at age 10. These
results are consistent with the MRI finding of bitemporal lobe atrophy,
the markedly decreased hippocampal volumes seen on MRI, and the
reemergence of the child's seizure disorder (left temporal lobe
discharges recorded on EEG) at age 10. In addition, our patient's pattern
of linguistic and verbal memory decline in conjunction with the results
from serial academic assessments, which indicate that she is no longer
developing reading, writing, and arithmetic skills at the normal rate
present at age 5, are consistent with the additional features of expressive
and receptive language disorder, combined with amnestic syndrome
characterized by the inability to make new declarative memories.
Many of the behavioral symptoms of Klüver–Bucy syndrome,
particularly the affective component, have been reported to respond
dramatically to carbamazepine [20–22]. Selective serotonin reuptake
inhibitors (SSRIs) have also been used for symptomatic treatment [23].
Our patient's hyperorality, hypersexuality, aggressiveness, inattention,
and hyperactivity were successfully treated with carbamazepine at
first and, later, in combination with clonidine, methylphenidate, and
lamotrigine.
Given the significant language and memory problems demonstrated
by serial neuropsychological assessment of our patient, along with the
cognitive deficits indicated by mental status examination (13/26) and
intelligence testing (3/26) in the pediatric KBS cases previously reported,
it is imperative that careful neuropsychological assessment and follow-
up be included in the treatment protocol of these children. This will not
only ensure accurate characterization of the disorder, but equally as
important, it will facilitate access to appropriate special education
remedial and compensatory services along with behavior management
programming under the eligibility category of “Other Health Impaired”
[24]. It will also help access private outpatient therapies if necessary.
Finally, assessment toward the end of high school will ease the transition
into vocational and technical school training if appropriate.
References
[1] Kluver H, Bucy PC. “Psychic blindness” and other symptoms following bilateral
temporal lobectomy in rhesus monkeys. Am J Physiol 1937;119:352–3.
[2] Klüver H, Bucy PC. An analysis of certain effects of bilateral temporal lobectomy in
the rhesus monkey with special reference in psychic blindness. J Psychol 1938;5:
33–40.
[3] Kluver H, Bucy PC. Preliminary analysis of functions of the temporal lobes in
monkeys. Arch Neurol Psychiatry 1939;42:979–1000.
[4] Terzian H, Dalle Ore G. Syndrome of Klüver and Bucy reproduced in man by
bilateral removal of the temporal lobes. Neurology 1955;5:373–80.
[5] Marlowe WB, Mancall EL, Thomas JJ. Complete Klüver–Bucy syndrome in man.
Cortex 1975;11:53–9.
[6] Lilly R, Cummings JL, Benson DF, Frankel M. The human Kluver–Bucy syndrome.
Neurology 1983;33:1141–5.
[7] Schraberg D, Welberg L. Kluver–Bucy syndrome in man. J Nerv Ment Dis 1978;166:
130–5.
[8] Janszky J, Fogarasi A, Magalova V, Tuxhorn I, Ebner A. Hyperorality in epileptic
seizures: periictal incomplete Klüver–Bucy syndrome. Epilepsia 2005;46:1235–40.
[9] Jha S, Patel R. Kluver–Bucy syndrome: an experience with six cases. Neurology
India 2004;52:369–71.
[10] Pradhan S, Singh MN, Pandey N. Klüver–Bucy syndrome in young children. Clin
Neurol Neurosurg 1998;100:254–8.
[11] Pitt D, Kriel R, Wagner N, Krach L. Kluver–Bucy syndrome following heat stroke in
a 12-year old girl. Pediatr Neurol 1995;13:73–6.
[12] Antunes NL, Souweidane MM, Lis E, Rosenblulm MK, Steinherz PG. Methotrexate
leukoencephalopathy presenting as Kluver-Bucy syndrome and uncinate seizures.
Pediatr Neurol 2002;26:305–8.
[13] Auvichayapat N, Auvichayapat P, Watanatorn J, Thamaroj J, Jitpimolmard S.
Kluver–Bucy syndrome after mycoplasmal bronchitis. Epilepsy Behav 2006;8:
320–2.
[14] Pestana EM, Gupta A. Fluctuating Kluver–Bucy syndrome in a child with epilepsy
due to bilateral anterior temporal congenital malformations. Epilepsy Behav
2007;10:340–3.
[15] Rossitch E, Oakes J. Kluver–Bucy syndrome in a child with bilateral arachnoid
cysts: report of a case. Neurosurgery 1989;24:110–2.
[16] Ozawa H, Sasaki M, Sugai K, et al. Single-photon emission CT and MR findings
in Klüver–Bucy syndrome after Reye syndrome. Am J Neuroradiol 1997;18:
540–2.
[17] Guedalai JSB, Zlotogorski Z, Goren A, Steinberg A. A reversible case of Kluver–Bucy
syndrome in association with shigellosis. J Child Neurol 1993;8:313–5.
[18] Wong VCN, Wong MTH, Ng THK, Chang CM, Fung CF. Unusual case of Kluver–Bucy
syndrome in a Chinese boy. Pediatr Neurol 1991;7:385–8.
[19] Utsunomiya H, Takano K, Okazaki M, Mitsudome A. Development of the temporal
lobe in infants and children: analysis by MR-based volumetry. Am J Neuroradiol
1999;20:717–23.
[20] Goscinski I, Kwiatkowski S, Polak J, Orlowiejska M, Partyk A. The Klüver–Bucy
syndrome. J Neurosurg Sci 1997;41:269–72.
[21] Hooshmand H, Sepdham T, Vries JK. Klüver–Bucy syndrome: successful treatment
with carbamazepine. JAMA 1974;229:1782.
[22] Stewart JT. Carbamazepine treatment of a patient with Klüver–Bucy syndrome.
J Clin Psychiatry 1985;46:496–7.
[23] Slaughter J, Bobo W, Childers MK. Selective serotonin reuptake inhibitor
treatment of post-traumatic Klüver–Bucy syndrome. Brain Inj 1999;13:59–62.
[24] Loring DW, Hermann BP, Cohen MJ. Neuropsychological advocacy and epilepsy.
Clin Neuropsychol 2010;24:417–28.