Journal of Neurology, Neurosurgery, and Psychiatry 1989;52:1260-1266

Rejection behaviour: a human homologue of the
abnormal behaviour of Denny-Brown and Chambers'
monkey with bilateral parietal ablation
ETSURO MORI, ATSUSHI YAMADORI
From the Neurology Service, Hyogo Brain and Heart Centre, Himeji, Japan
SUMMARY A unique behavioural syndrome in humans followed two separate strokes involving both
parietotemporal regions. The behavioural alterations resemble those of Denny-Brown and
Chambers' monkey with bilateral ablation of the parietal lobe which were characterised by strong
withdrawal or refusal to be touched on the limbs and head. In both humans and animals, touch on the
limbs or head elicited exaggerated withdrawal movements and refusal to be touched on the lips and
tongue resulted in difficulty in feeding. These behavioural alterations can be interpreted as loss of
exploratory activities towards extrapersonal space, or more positively, as rejection of contact with the
environment. This rejection behaviour in which tactile, visual, and/or gustatory exploration
tendencies are altered, is a counterpart of human frontal lobe syndrome and human Kluver-Bucy
syndrome.
In their series of studies on parietal lobe function, frontal lobe damage.23 The pathological grasping
Denny-Brown and Chambers' noted that ablations of behaviour has been interpreted as a feature of exagthe parietal lobe in the rhesus monkey resulted in gerated tactile exploratory tendency inherent in
remarkable behavioural alterations. Following parietal lobe function.'3 This interpretation has been
unilateral ablation of the parietal lobe, the animal amply confirmed by monkey experiments.' Recently
developed distortion of behaviour characterised by reported behavioural syndromes, such as compulsive
avoiding reactions to stimuli in the opposite somatic manipulation of tools4 and utilisation behaviour,5 can
and visual fields. After bilateral ablation the whole also be interpreted as a type of manual grasping
behaviour of the animal changed so that withdrawal behaviour in more elaborate form. In all these synwas the response to any stimulus, including food dromes, the responsible lesions have been related to
which normally attracted the animal. The animal with the frontal lobe.
bilateral ablation became nervous and restless with
On the other hand, bilateral temporal lobe damage
any form of stimulation, backing away from the has been known to produce the Kluver-Bucy synstimulus. There was great sensitivity to contact with drome.6 The syndrome includes psychic blindness,
exaggerated withdrawal of head or limbs if these were strong tendencies to examine all objects orally, an
touched (tactile avoiding reaction). Although the irresistible impulse to touch, loss of normal anger and
animal appeared not to see an object approaching him fear responses and increased sexual activity.6 This
in the acute stage after operation, avoiding reaction syndrome, originally reported with experimental monthereafter was elicited by a visual stimulus (visual keys, was also confirmed in human patients with the
avoiding reaction). The avoiding reaction of the lips same distribution of lesions.7 Part of the syndrome,
led to great difficulty in getting the animal to open its such as hypermetamorphosis can be interpreted as a
mouth and feed.
manifestation of exaggerated visual, tactile and oral
Avoiding responses due to parietal lobe damage are exploring tendencies as a result of the loss of visual
dynamically related to the grasping behaviours due to avoiding reaction.'
Thus clinical syndromes are known which are
almost equivalent to the monkey syndromes in frontal
Correspondence to: Etsuro Mori, Neurology Service, Hyogo Brain and temporal lobe damage. However, we still do not
and Heart Centre at Himeji, 520, Saisho-Ko, Himeji, 670, Japan.
know the human equivalent of the monkey parietal
lobe syndrome produced by Denny-Brown and ChamReceived 15 November 1988 and in revised form 17 May 1989.
Accepted 14 June 1989
bers. Some researchers have expressed doubts that
1260

1261

Rejection behaviour: abnormal behaviour of Denny-Brown and Chambers' monkey with parietal ablation

F'ig l Contiguous CTsections of patient 1. Left appears to be on the left.
parietal lobe lesions could induce indifference or
escape behaviour in response to tactile, visuo-tactile or
visual stimuli.5 Although Denny-Brown3 maintained
that repellent apraxia in man ranked with avoiding
reaction in monkeys, it was rather different from the
behaviour observed in experimental animals. The
former is only a simple sensorimotor abnormality,89
that is, a manifestation of deafferentation, which
appears following lesions in the posterior column of
the spinal cord'0°" or thalamus,'2 while the latter is
highly integrated and elaborated and involves alteration of an individual's whole attitude to their environment. We describe four patients with strokes in the
parietal lobe of both hemispheres whose changes in
behaviour are comparable to that of Denny-Brown
and Chambers' monkey with bilateral ablation of the
parietal lobe. The changes in their behaviour were
characterised by strong withdrawal from tactile
stimuli. We propose to call this new human behavioural syndrome 'rejection behaviour'.

interpreted as cortical blindness or severe visual inattention.
He also appeared to be deaf but sometimes responded to loud
noises. He was usually bad tempered.
A light touch consistently produced withdrawal movements in the head and limbs. There was no evidence that a
light touch on the body produced a painful sensation.
Because of these reactions, nursing was difficult and feeding
impossible. The lips became tightly closed and he averted his
face when food was placed on his lips. When a piece of food
was pushed into his mouth, he would spit it out as if the taste

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...
...

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.....

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Case reports
Patient 1. A 72 year old right-handed man, with a history of
atrial fibrillation, suddenly developed agitated delirium and
was admitted to our hospital. His family had not noticed any
change in his behaviour before this episode. On admission, he
was agitated, resistant and restless. His speech was incoherent. He did not comprehend spoken language at all.
Cranial nerves other than visual acuity, muscle strength,
tendon reflexes and plantar responses were normal. Computed tomography (CT) of the brain showed two hypodense
areas: one was a well-demarcated hypodensity in the right
parietotemporooccipital region consisting of an old infarction in the territory of the inferior division of the right middle
cerebral artery, and the other a faint hypodensity in the left
parietotemporal region consistent with an acute infarction of
the inferior division of the left middle cerebral artery (fig 1).
Within a few days, his initial agitated behaviour improved
considerably. He was logorrhoeic, insomniac at night and
incontinent but he was able to walk without help. However,
he did not recognise any objects placed in front of him and
did not make eye contact. His visual disturbance was

.J
X~~~~~~~~.

..

Fig 2 Coronal sections of the brain ofpatient 1. Old
infarctions of the parietotemporooccipital region of both
hemispheres. Relatively new infarctions also affecting the left
rolandic area.

1262

Mori, Yamadori

Fig 3 Contiguous CT sections ofpatient 2. Left appears to be on the left.

Patient 1

was bitter. His gag reflex was within normal range and
movements of the soft palate, lips and tongue were all

normal, as was swallowing. It was unknown whether gustation was preserved. Intravenous nutrition and tube feeding
/
were required for a month. This rejection behaviour lasted
N%,,.
~
~
for approximately 40 days then gradually subsided and he
was then able to feed himself. He was discharged home two
months after the onset.
Six months later, he developed left hemiparesis following
infarction in the right paracentral region and one year later
he died of gastric cancer. Neuropathological examination
Patient 2
revealed: old ischaemic lesions with cystic change of the right
parietotemporooccipital region; an old infarction of the left
parietotemporal region; an old infarction of the right Rolandic area; a small, old infarction in the right cerebellar
/
)
,..)_- hemisphere (fig 2). Although moderate atherosclerosis was
found in the basilar artery, occlusion was not apparent in the
major cerebral arteries. The infarction of the right
parietotemporal region affected the inferoposterior portion
of the inferior parietal lobule, the posterior portion of the
Patient 3
superior temporal gyrus and the anterolateral part of the
occipital lobe. In the left hemisphere, the whole of the inferior
parietal lobule, the posterior part of the parietal operculum,
the posterior part of the superior temporal gyrus and the
*
....~~~~~~~~~~
~anterolateral part of the occipital lobe were involved. In both
*
hemispheres, the Heschl gyrus was destroyed and the optic
raitoswere disconnected (fig 1).

Patient 2. A 71 year old right-handed hypertensive house-

Patient 4

Fig 4 Schematic representation of lesion extent. Drawings
based on material at necropsy in patient 1 and reconstructed
from the CT using Mazzochi and Vignolo's method'3 in
patients 2, 3, and 4. These show a common lesion site in the
inferior parietal gyrus and posterior part of the superior
temporal gyrus of both the hemispheres.

wife was first admitted to this unit with a two week history of
speech disturbance and altered behaviour. Examination
revealed right homonymous hemianopia, right-sided mild
hemisensory deficits, alexia with agraphia, constructional
disability, ideomotor apraxia and mild right-sided visual
neglect. CT showed a hypodensity in the left parietotemporal
region consistent with an infarction in the territory of the
inferior division of the left middle cerebral artery. She was
discharged with a diagnosis of thrombotic stroke. Six months
later, she suddenly became unconscious and was readmitted.
She was stuporose. There were conjugate rightward ocular
deviation, left hemiparesis, hyperreflexia on the left side and
extensor plantar response on the left side. CT on the second
admission showed a massive subcortical haematoma in the
right parietal lobe as well as the previous left parietotemporal
infarction (fig 3) Two weeks later, a burr hole was made and
the haematoma was removed.

Rejection behaviour: abnormal behaviour ofDenny-Brown and Chambers' monkey with parietal ablation

rig

1263

Cuontiguous us sectons ojpatien J. .ejauppears u oe on Ine eJL.

After remaining in a critical condition for a few weeks, she
regained consciousness and muscle strength of the limbs of
the left side. However, as her recovery progressed, behavioural abnormalities became evident. She was restless,
incontinent, had insomnia, and was markedly logorrhoeic.
Her speech was irrelevant and incoherent and she appeared
to have both cortical blindness and deafness. Although she
was frequently irritable, her facial expression appeared
normal. Light touch consistently produced withdrawal
movements of the limbs and head but did not seem to cause
pain. When feeding was attempted, her lips remained firmly
closed and she turned her face away. If the food was put into
the mouth, she would push it out with the tongue. There was
no apparent swallowing difficulty. Movements of the lips,
soft palate and tongue were normal. It was not possible to test
gustatory sensation. As a result it was necessary to feed her by
nasogastric tube. This abnormal behaviour lasted for over a
year.
An analysis of the CT scans (using the method described by
Mazzochi and Vignolo'3) showed that, in the left hemisphere
damage had occurred to the whole of the inferior parietal
lobule, the superior temporal gyrus and the parietal operculum. In the right hemisphere the areas affected were: the
whole of the inferior parietal lobule, the inferior half of the
paracentral gyri, and the posterior part of the superior
temporal gyrus (fig 4).
Patient 3. A woman aged 72 years with a history of sick

sinus syndrome was admitted to this unit because of the
sudden onset of right hemiplegia. She had global aphasia,
dense right hemiplegia, right hemisensory deficits, right
homonymous hemianopia and conjugate leftward ocular
deviation. Emergency angiography showed a distal occlusion
of the left internal carotid artery. CT the day after showed a
large perisylvian hypodensity consistent with an infarction of
the territory supplied by the left middle cerebral artery. On
the seventh day, the conjugate ocular deviation reversed its
direction. Repeated CT showed another hypodensity in the
right parietotemporal region indicating cerebral embolism in
the region of the inferior division of the right middle cerebral
artery (fig 5).
For a few weeks her condition was critical. She then
became awake and her conjugate ocular deviation disappeared. She was incontinent and had insomnia and she
restlessly moved her limbs. The right hemiplegia and global
aphasia remained unchanged. She was mute and did not
understand any verbal commands. She appeared to have
cortical blindness and deafness. Her affect was flat and she
withdrew her hand whenever it was touched. When touched
on her left palm, she extended her fingers and wrist, to avoid
the stimulus. She pushed food out with the tongue when it
was forced into her mouth. She was fed through a nasogastric
tube. Swallowing appeared normal. Gustation seemed
preserved to some degree. When syrup was placed on her
tongue, she appeared to appreciate the taste and when brine

Fig 6 Contiguous CTsections ofpatient 4. Left appears to be on the left and right on the right.

1264
water was given she spat it out. Three months after the onset
there was no improvement and she was transferred to a local
hospital.
The CT scan analysis showed the lesion in the left
hemisphere extended to the inferior frontal gyrus, paracentral gyri, inferior parietal lobule, and superior and middle
temporal gyri; the lesion in the right hemisphere involved the
parietal operculum, inferior parietal lobule and the whole of
the superior temporal gyrus (fig 4).
Patient 4. A 73 year old right-handed woman was admitted
to this unit with right-sided convulsions. Three months
before admission she had had a cerebral infarction and
Wernicke aphasia and had been admitted elsewhere for six
weeks. CT disclosed haemorrhage in the left parietotemporal
subcortical region as well as a hypodensity in the left
parietotemporooccipital region consistent with the previous
cerebral infarction. After the seizure was controlled there was
right homonymous hemianopia and severe Wernicke aphasia
with no comprehension of language. Angiography was
performed on the tenth day and showed a dural arteriovenous malformation in the left posterior fossa. She then
became restless, unable to sleep and incoherent. Her
behaviour then changed considerably and she became irritable and unresponsive to bright light or loud noises. If
touched on her limb, she would withdraw from the contact.
Although she responded to light touch on her body with
grimacing and crying, the appearance was quite different
from that observed when truly painful stimuli were given.
Therefore, it was unlikely that the light contact elicited a
painful sensation. Touch on the face consistently produced
withdrawal movement of her head. When her lips were
touched, she would firmly close them. If food was put into her
mouth, she would push it out with the tongue. Because food
was refused intravenous nutrition and tube feeding were
maintained. Our experience ofthe similar syndromes in those
patients described above made us suspect a possibility of
bilateral parietotemporal lesions. Indeed, the second CT on
the 13th day showed a recurrence of a cerebral infarction
involving the right parietotemporal region (fig 6). Withdrawal movements of the hands from tactile stimuli
decreased by the end of the second week. However, avoiding
movements of the face and lips persisted, and refusal to take
food continued. She would only take a certain type of fruit
and ice cream. The dural arteriovenous malformation was
completely removed one month later. However, her
behaviour pattern remained unchanged.
The analysis of the CT scans indicated that lesions in the
left hemisphere extended to the inferior parietal lobule,
superior and middle temporal gyri and occipital lobe, whilst
lesions in the right hemisphere involved the parietal operculum, inferior parietal lobule and the whole of the superior
temporal gyrus (fig 4).

Discussion
Bilateral parietotemporal lobe damage resulted in
remarkable behavioural changes in four patients.
Touching the limbs and head produced withdrawal
behaviour. When touched on the hand, the patients
quickly withdrew from the stimulus. These withdrawal
movements were not a response to pain sensation
which would occur with a thalamic syndrome. They

Mori, Yamadori
refused food by closing the mouth tightly or by
averting the face. If the food was placed in the mouth,
the patients would expel it with the tongue. As there
was no consistent reaction, it was unlikely that refusal
to take food was due to an alteration of gustatory
sense. This behavioural distortion must be a reflection
of the alteration of the patient's attitude towards the
environment. Withdrawal, or more positively,
avoidance became a dominant response to contact. To
the observer, these patients gave a strong impression
that they were actively "rejecting" all external contact.
Thus, we propose to call this peculiar symptom
complex "rejection behaviour".
Such behaviour is equivalent to those responses
observed in Denny-Brown and Chambers' experiments on animals with bilateral ablation of the parietal
lobes. Operative removal of the parietal lobes in the
monkey induced a lasting change in the behaviour of
an animal characterised by similar withdrawal
activity, associated with the facial expression,
irregular exaggeration and repetition of withdrawal
movements characteristic of anxiety.' A light touch on
a hand or foot led to exaggerated but delicate withdrawal from the stimulus (tactile avoiding). When
tested with objects in the visual field the animal would
look away and push away with the hand (visual
avoiding). Avoiding reaction of the lips led to great
difficulty in feeding in the acute postoperative stage.
Even after a long survival some difficulty remained in
getting the animal to open its mouth.' Therefore, it is
conceivable that the rejection behaviour is homologous to the behaviour of the Denny-Brown and
Chambers monkey. Associated emotional changes
such as irritability, restlessness and insomnia, were
also seen in the experimental animals.
There were, however, differences between the
experimental animal and the patient with strokes. In
the monkey, unilateral parietal damage produced
avoiding reaction in the contralateral limbs,' whilst in
patients with strokes a unilateral parietotemporal
lesion did not produce any changes in exploratory
behaviour other than unilateral neglect. This may be
either due to species difference or to differences in the
size of the lesion (in our patients the superior parietal
lobule was always spared). Although detailed assessments were impossible because of gross deficits of
higher cortical function, there was no doubt that
severe visual and auditory disturbances of central
origin, that is, cortical blindness and deafness, were
present in all our patients. These features were not
recorded in the experimental animal. Concurrent
damage of visual, auditory and linguistic functions
may be a necessary condition for the appearance of
rejection behaviour in humans. It is possible that,
when communicative channels with the environment
other than the tactile modality are open, this tactile

Rejection behaviour: abnormal behaviour ofDenny-Brown and Chambers' monkey with parietal ablation 1265
avoiding tendency may be easily inhibited by some and visuospatial) processing." Thus rejection
kind of compensatory mechanism. A relationship behaviour is an extreme form of the parietal lobe
between gustatory alteration and rejection of food syndrome and can be interpreted as a total loss of
remains uncertain. Gustatory alteration was not exploration to the environment, or more positively, as
described in the experiments of Denny-Brown and a refusal of contact with the environment. It is a
Chambers, but it is quite possible that parietal lesions counterpart of the frontal lobe syndrome and the
may change gustation. The gustatory sensation is Kluver-Bucy syndrome in which tactile and visual
thought to reside in the anterior Sylvian cortex'4 or exploration are hyperactive. Some of the frontal lobe
syndromes including oral tendency, sucking response,
parietal operculum.'5'6
In the present series, common lesions always in- bilateral instinctive grasp reaction,2 compulsive
cluded the inferior parietal lobule and posterior part of manipulation of tools,4 utilisation behaviour5 and
the superior temporal gyrus suggesting the importance some of the main fragments of the Kliiver-Bucy
of these lesions in producing rejection behaviour (fig syndrome including hypermetamorphosis, hyper4). The experiments of Denny-Brown and Chambers' orality and hyperbulimia are in sharp contrast with the
indicated a relatively greater release ofvisual avoiding main symptoms of rejection behaviour. In addition,
reaction by ablation of the posterior parietal lobe emotional characteristics of irritability and temper
(including the posterior part of the superior temporal observed in rejection behaviour are in contrast with
sulcus), of tactile and nociceptive reactions by antero- the placidity and apathy of those with frontal lobe or
lateral ablation (namely, the postcentral gyrus and Kluver-Bucy syndromes.
The behavioural syndrome we describe could be
parietal operculum) and of all types of avoiding
reaction by ablation of the intraparietal area (area 7). called the "Denny-Brown Chambers syndrome." This
The areas in the monkey brain which can be con- behaviour is occasionally observed in severe
sidered homologous to the inferior parietal lobule of neurological diseases. More attention should be given
the human brain are the inferior parietal lobule and to the role of the parietal lobe in human behaviour.
the depths of the superior temporal sulcus.'7 In From a clinical point of view, the main problem in
addition, the equivalent area of monkey intraparietal rejection behaviour is care and nursing. It is imporarea is considerably larger in the human brain.'8 tant, therefore, for those who care for patients with
Brodmann'9 pointed out that his monkey area 7 diseases that predominantly affect the parietal lobe to
should be thought of as an undifferentiated area recognise this rejection behaviour.
comparable to his human areas 7, 39 and 40. Therefore, the extent of lesions indicated in this study is
comparable to ablation of the posterior parietal and References
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