Psychosomatics 2011:52:563–567

© 2011 The Academy of Psychosomatic Medicine. Published by Elsevier Inc. All rights reserved.

Case Reports
A Case Of Utilization Behavior and Hyperorality Following
Bilateral Anterior Cerebral Artery Infarct Partially Responsive
to Carbamazepine: Can Both Behaviors Be Attributed To
Lesions In Different Frontal Lobe Circuits?
David R. Spiegel, M.D., Kevin Lamm, M.D.

L

hermitte (1983) coined the term “utilization behavior” (UB) to define a neurobehavioral syndrome in
which the visuo-tactile presentation of objects compels
patients to grasp and use them, despite the fact that they
have not been instructed to do so. The author suggested
that UB was the consequence of frontal lobe damage.1
There are various interpretations as to the pathophysiology
that brings about UB. Authors have described UB as an
executive function deficit,1 intimating impairment in dorsolateral frontal-subcortical circuits.2 Yet, others have proposed disconnection between frontal and parietal lobe circuits or intra-frontal lobe pathology.3
Hyperorality and “bulimic type eating” (BTE) are
symptoms of Kluver-Bucy Syndrome (KBS).4 While typically occurring after bilateral amygdala lesions/removal,
others have suggested that symptoms of KBS may develop
due to selective neurotoxicity in the basolateral amygdala
and its cortical connections.5 Furthermore, the circuit between amygdala and cortex are reciprocal.6 Thus, disruption of a frontal-amygdalar circuit, with the latter projecting to the hypothalamus,7 may result in the production of
Kluver-Bucy symptoms.8
We present a case of a woman with a bifrontal craniotomy and subsequent anterior cerebral artery cerebrovascular accident who developed manifestations of UB
and Kluver-Bucy symptoms of hyperorality and BTE. We
treated this patient with carbamazepine (CBZ), with the
latter symptoms significantly improving, but the former
essentially unchanged. We suggest that it is possible that
this result may have occurred because while UB may not
improve with CBZ, both bulimic type eating9 and symptoms of KBS have been reported to respond to treatment
with CBZ.10
Psychosomatics 52:6, November-December 2011

Case Report

Ms. A, a 29-year-old female was admitted to the physical
medicine and rehabilitation service of our hospital after
treatment of a bifrontal parafalcine meningioma. She had
no significant past medical/psychiatric/substance abuse
history and initially presented after two episodes of altered
mental status. Magnetic resonance image (MRI) was performed that revealed a large anterior fossa mass. She underwent embolization of two blood vessels supplying her meningioma, followed by a bifrontal craniotomy for resection of
the meningioma. After 4 hours, she became nonverbal and
stopped moving all extremities. MRI of the head showed
bilateral anterior cerebral artery distribution infarct involving
the parasagital frontal lobes and left caudate nucleus. After a
7-week hospital stay, Ms. A was transferred to our hospital
for further rehabilitation services.
Four days after transfer, the psychiatric consultation
and liaison team was consulted for “difficult behavior and
having periods of significant agitation.” Additionally, the
staff reported that they had begun feeding her because
when left alone with her meal tray she would eat so
ravenously that she would choke. On our initial consultation, Ms. A was fully awake, though oriented only to
person. She had significantly constricted affect and inReceived December 8, 2010; revised January 9, 2011; accepted January 10,
2011. From Dept. of Psychiatry and Behavioral Sciences, Eastern Virginia Medical School, Norfolk, VA.Send correspondence and reprint
requests to David R. Spiegel, M.D., Dept. of Psychiatry and Behavioral
Sciences, Eastern Virginia Medical School, 825 Fairfax Avenue, Norfolk, VA 23507. e-mail: spiegedr@evms.edu
© 2011 The Academy of Psychosomatic Medicine. Published by
Elsevier Inc. All rights reserved.

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Case Reports
creased speech latency, and during the interview she
would bite a stuffed animal she was holding. While testing
for grasp and rooting reflexes the patient pinched the examiner and tried to bite the examiner’s hand. Her Mini
Mental State Examination (MMSE)11 score was 19. When
asked specific questions she would often look around the
room for answers. For example, when asked who the
president was, she would read the interviewer’s badge or
point to people in the room. Despite not knowing these
answers, she seemed unconcerned. Further, she would take
a pen and write on paper if it was in front of her, but would
continue to attempt to write even after the paper was taken
away. Ms. A made several attempts to drink from any
empty cup if it was within reach. She scored 3 on severity
for the following subsections on Neuropsychiatric Inventory Questionnaire (NPI-Q)12: apathy/indifference (A/I),
disinhibition (D), and appetite/eating (A/E), while scoring
a 1 on the agitation/aggression (A) and irritability/lability
(I) subsections. Her laboratory work-up was unremarkable, but an electroencephalogram showed continuous
slowing over the frontal region, consistent with lesions.
Ms. A was started on, and titrated to, CBZ 400 mg
BID (blood level of 9 mcg/mL) in an attempt to treat
disinhibited behaviors. While her MMSE remained the
same, A/E and D subscales decreased to 1, A/I score
remained at 3 and A, I subscales continued to score 1.
Interestingly, improvement in eating behavior occurred
such that staff no longer had to feed her for her protection;
however, her previously mentioned behavior with the pen
and empty cup did not attenuate. Eventually Ms. A was
discharged to hospice care due to formation of deep vein
thrombosis/pulmonary emboli and she expired within 1
month of discharge.

Discussion

Phenomenolgy. Our case report seems to demonstrate two
groups of symptoms, which, in part, may be interconnected: UB and hyperorality and bulimic-type eating. Various frontal-subcortical circuit syndromes are known to
include apathy, disinhibition, and executive function deficits, including impersistence and stimulus-bound behavior. Lhermitte introduced the term “utilization behavior,”
which he observed among patients affected with left or
right unilateral, or bilateral, frontal lesions. He explained it
as an extension of bilateral manual grasping behavior
(“magnetic apraxia”), and believed that UB is the auto564

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matic elicitation of instrumentally correct, yet highly exaggerated and/or inappropriate motor responses to environmental cues/objects.13
For clarity’s sake, a further delineation of hyperorality, pathologic grasp (reflex), and BTE, will be defined.
Hyperorality describes nonselective placing of edible or
inedible objects to a person’s mouth.4 Pathologic grasp
(i.e., reflex) may be described as the automatic tendency to
grip objects or other stimuli. Additionally, attempts to
withdraw the stimulating object may result in strengthening of the grasp.13 Finally, BTE is described as eating an
amount of food in a discrete time that is considered excessive in view of the situational context, with the associated feature of eating more rapidly than normal.14
Patients with frontal lobe damage often appear to be
easily distracted and strongly influenced by irrelevant external stimuli, such that they have difficulty behaving in
accordance with the plans or intentions that they have
created. Theoretically, UB is explained as resulting from a
loss of frontal inhibitory control over more automatic behaviors, i.e., an imbalance between frontal (internally generated) and parietal (externally or environmentally driven)
systems. Abnormal behaviors may be triggered by externally oriented systems responsive to environmental input,
if there is a loss of frontally-based inhibitory controls that
mediate more purposeful, volitional, and internally generated behavior.
Certain behaviors of Ms. A may be attributed to UB,
such as her persistent attempts to drink from an empty cup
and continued writing movements when the paper was
removed. Interestingly, neuropathologic observations by
Lhermitte and others reported that lesions of the orbital
surface of the frontal lobe, and sometimes the head of the
caudate nucleus, were involved in UB. Thus, our patient’s
UB is supported, in part, by structural findings on MRI.
The target symptoms that responded to CBZ treatment
were the hyperorality and BTE, with near choking episodes. Certainly, hyperorality and BTE could be attributed
to UB, i.e., rapid unrestrained eating of food present in the
environment. However, hyperorality and BTE are also
Kluver-Bucy symptoms. Typically associated with temporal lobe pathology, the entire syndrome has been described
elsewhere.5 Nonetheless, Ms. A did not have identified
temporal lobe pathology on MRI. We propose a potential
different pathophysiologic explanation for her hyperorality and BTE, based upon the lack of response of all other
UB symptoms to CBZ.
Anatomy/Physiology. Neuroanatomically, it has been
reported that stereotypic behavior and change in behavior
Psychosomatics 52:6, November-December 2011

Spiegel and Lamm
related to food, reflects the involvement of a common
network—namely, the orbitofrontal cortex, temporal pole,
and amygdala.15 Additionally, neural projections exist
from distinct amygdalar nuclei and orbitofrontal cortex to
the lateral hypothalamus, a key center for the initiation of
feeding. What is being encoded by the projections from
amygdala and orbitofrontal cortex to the hypothalamus
remains to be established. It has been proposed that these
connections may convey a nonspecific reward signal that
blindly increases appetitive behaviors.16
Both the temporal pole and amygdala are heavily interconnected with the orbitofrontal lobe with the amygdala having reciprocal connections with both orbitofrontal and anterior cingulate cortex.15 The orbitofrontal cortex has long been
associated with regulating inhibitory control and damage
leads to a failure to inhibit inappropriate responses.2 Additionally, lesion studies in rats demonstrate that efferent projections from the posterodorsal amygdala to the hypothalamus leads to BTE, obesity, and sexual dysregulation.17 Thus,
while amygdalofugal connectivity may be a final common
pathway leading to hyperorality/BTE, amygdala dysregulation can be precipitated by frontal lobe lesions, the latter
occurring in our patient.
FIG. 1.

Treatment. We chose CBZ because of past reports of
its utility for the treatment of disinhibition in neuropsychiatric patients18 and BTE9— our “a priori target symptoms.” One of several possible mechanisms of action of
CBZ is as an augmenter of the gamma amino butyric acid
(GABA) system, which is primarily inhibitory in function.18 Additionally, cortical neurons project glutamatergic
efferents to the amygdala (and visa-versa). It is tempting to speculate that a frontal lobe lesion could result in
decreased excitatory transmission to the amygdala, resulting in a hypofunctioning amygdala with resultant
hyperorality/BTE. Thus, increasing inhibitory transmission via CBZ could inhibit inhibitory transmission resulting in successful treatment of our patient’s altered
eating behavior. However, it is unclear if transmission
between “amygdalofrontal” or amygdalofugal circuits
are mono- or polysynaptic in nature. Thus, a direct
effect of CBZ on this circuit can only be speculative.19
Furthermore, the prefrontal cortex has direct projections
to the lateral hypothalamus. Thus, it is also possible that
amygdala/medial temporal lobe is completely bypassed
and that CBZ might directly affect prefrontal-hypothalamic pathways.16 (see Figure 1).

Schematic of the Discussed Interactions Between Frontal Cortex, Amygdala, and Hypothalamus.

OPro ⴝ orbitofrontal area; D24 ⴝ dorsal area 24; M25 ⴝ medial area 25; L ⴝ lateral nucleus; BL ⴝ basolateral nucleus; IM ⴝ intercalated
masses; C ⴝ central nucleus; PAG ⴝ periaqueductal gray matter; (ⴙ) ⴝ excitatory; (ⴚ) ⴝ Inhibitory; VMN ⴝ ventromedial nucleus.

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Case Reports
CBZ had no effect on apathy or Ms. A’s UB. While an
explanation for this is beyond the scope of this manuscript,
in the frontal–subcortical circuits, the corticostriatal information processing is modulated by different neurotransmitter systems. Dopaminergic neurons from the substantia
nigra/midbrain, project to the striatum and affect all frontal–subcortical functions. There are nigral connections
with the limbic circuits, which are rich in dopamine (DA)
(DA3 and DA4) receptor subtypes. This allows the interaction between emotional input and motor activity and
motivation. This anatomical structure forms the basis for
multiple actions of dopaminergic agents including effects
on motivation and behavior. As one of the roles of anterior
cingulated circuit is to subserve motivation, lesions in this
circuit can cause apathy; hence, the role potential of DA
agonists, not medications that facilitate GABA transmission, for the treatment of apathy.
Additionally, certain studies indicate high levels of
UB in approximately one-half of the children with Attention Deficit/Hyperactivity Disorder (ADHD),
whereas almost no such behavior was observed in controls. Levels of UB were statistically associated with the
severity of hyperactivity.20 Positron emission tomography studies of DA receptor binding have implicated
abnormality of DA at the level of the midbrain in adolescents, and at the level of frontal lobe in adults, with
ADHD. These findings have been interpreted as suggesting that the frontal dopaminergic abnormality seen
in adults with ADHD occurs secondary to a subcortical

dopaminergic deficit interacting with neurodevelopmental changes. Thus, medications that enhance dopaminergic transmission might be more suitable for treating UB,21 which, in our patient, was unaffected by CBZ.
In conclusion, we propose that both UB and certain
Kluver-Bucy symptoms, such as hyperorality and BTE,
can develop as a result of frontal lobe pathology. It would
certainly seem that our patient’s hyperorality/BTE did not
occur due to direct medial temporal cortex/amygdalar lesions. However, the frontal lobes are a complex and highly
interconnected area of the brain with five known parallel
frontal-subcortical neuronal circuits.2 Thus, since there are
demonstrated reciprocal frontal-amygdalar circuits as well
as amygdalofugal pathways, indirect involvement of the
amygdala through frontal lobe pathology (with the latter
occurring in Ms. A), and subsequent involvement of lateral hypothalamus, could also result in hyperorality and
BTE. Similarly, with bidirectional frontal-hypothalamic
circuits, frontal lobe lesions can also directly affect lateral
hypothalamus, potentially resulting in BTE. Therein lies the
major limitation of our case report, in that while these multiple
circuits do exist, whether lesions in any/all of these circuits do
result in hyperorality (or other Kluver-Bucy symptoms) would
require further research, perhaps with functional rather than
structural scans. Furthermore, we believe that larger scale randomized trials are warranted in treating frontal-hypothalamic or
frontal-amygdalo-hypothalamic circuit-induced Kluver-Bucy
symptoms, such as hyperorality, or BTE with anticonvulsants,
such as CBZ.

References
1. Besnard J, Allain P, Aubin G, et al: Utilization behavior: clinical
and theoretical approaches. J Int Neuropsychol Soc 2010;16:
453– 462
2. Tekin S, Cummings JL: Frontal-subcortical neuronal circuits
and clinical neuropsychiatry: an update. J Psychosom Res 2002;
53:647– 654
3. Eslinger PJ: The anatomic basis of utilisation behaviour: a shift
from frontal-parietal to intra-frontal mechanisms. Cortex 2002;
38:273–276
4. Mendez MF, Foti DJ: Lethal hyperoral behaviour from the Kluver-Bucy syndrome. J Neurol Neurosurg Psychiatry 1997; 62:
293–294
5. Hayman LA, Rexer JL, Pavol MA, et al: Kluver-Bucy syndrome
after bilateral selective damage of amygdala and its cortical
connections. J Neuropsychiatry Clin Neurosci 1998; 10:354 –
358
6. Stalnaker TA, Roesch MR, Calu DJ, et al: Neural correlates of
inflexible behavior in the orbitofrontal-amygdalar circuit after cocaine exposure. Ann N Y Acad Sci 2007; 1121:598 –
609

566

www.psychosomaticsjournal.org

7. Petrovich GD, Setlow B, Holland PC, et al: Amygdalo-hypothalamic circuit allows learned cues to override satiety and promote eating. J Neurosci 2002; 22:8748 – 8753
8. Winstanley CA, Theobald DE, Cardinal RN, et al: Contrasting
roles of basolateral amygdala and orbitofrontal cortex in impulsive choice. J Neurosci 2004; 24:4718 – 4722
9. McElroy SL, Guerdjikova AI, Martens B: Role of antiepileptic
drugs in the management of eating disorders. CNS Drugs 2009;
23:139 –156
10. Stewart JT: Carbamazepine treatment of a patient with Kluver-Bucy syndrome. J Clin Psychiatry 1985; 46:496 – 497
11. Folstein MF, Folstein SE, McHugh PR: “Mini-Mental State.” A
practical method for grading the cognitive state of patients for
the clinician’’. J Psychiatr Res 1975;12:189 –198
12. Kaufer DI, Cummings JL, Ketchel P, et al: Validation of the
NPI-Q, a brief clinical form of the Neuropsychiatric Inventory.
J Neuropsychiatry Clin Neurosci 2000;12:233–239
13. Archibald SJ, Mateer CA, Kerns KA: Utilization behavior: clinical manifestations and neurological mechanisms. Neuropsychol
Rev 2001; 11:117–130

Psychosomatics 52:6, November-December 2011

Spiegel and Lamm
14. Treasure J, Claudino AM, Zucker N: Eating disorders. Lancet
2010; 375:583–593
15. Ghashghaei HT, Hilgetag CC, Barbas H: Sequence of information processing for emotions based on the anatomic dialogue
between prefrontal cortex and amygdala. Neuroimage 2007; 34:
905–923
16. Seymour B: Carry on eating: neural pathways mediating conditioned potentiation of feeding. J Neurosci 2006; 26:1061–1062
17. Kile SJ, Ellis WG, Olichney JM, et al: Alzheimer abnormalities of
the amygdala with Kluver-Bucy syndrome symptoms: an amygdaloid variant of Alzheimer disease. Arch Neurol 2009; 66:125–129
18. Spiegel DR, Qureshi N: The successful treatment of disinhibition due to a possible case of non-human immunodeficiency

Psychosomatics 52:6, November-December 2011

virus neurosyphilis: a proposed pathophysiological explanation
of the symptoms and treatment. Gen Hosp Psychiatry 2010;
32:221–224
19. Cohen MX, Elger CE, Weber B: Amygdala tractography predicts functional connectivity and learning during feedbackguided decision-making. NeuroImage 2008; 39:1396 –
1407
20. Archibald SJ, Kerns KA, Mateer CA, et al: Evidence of utilization behavior in children with ADHD. J Int Neuropsychol Soc
2005 ;11:367–375
21. Roth RM, Saykin AJ: Executive dysfunction in attention-deficit/
hyperactivity disorder: cognitive and neuroimaging findings.
Psychiatr Clin North Am 2004; 27:83–96, ix

www.psychosomaticsjournal.org

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