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European Child & Adolescent Psychiatry

10:7990 (2001) Steinkopff Verlag 2001 ORIGINAL CONTRIBUTION

C. Njiokiktjien Disordered recognition of facial identity


A. Verschoor
L. de Sonneville and emotions in three Asperger type
C. Huyser
V. Op het Veld autists
N. Toorenaar

Accepted: 18 January 2000


j Abstract In this report we aim pathogenetic symptom for the
to explore severe decits in facial autistic behaviour in the three
affect recognition in three boys all boys. Prosopagnosia, the absent
of whom meet the criteria of facial and bodily expression, and
Asperger's syndrome (AS), as well speech prosody were important
as overt prosopagnosia in one (B) but varying co-morbid disorders.
and covert prosopagnosia in the The total clinical picture of non-
remaining two (C and D). Subject verbal disordered communication
B, with a familially-based talent of is a complex of predominantly
being highly gifted in physics and bilateral and/or right hemisphere
mathematics, showed no interest cortical decits. Moreover, in B,
in people, a quasi complete lack of insensitivity to pain, smells, nois-
comprehension of emotions, and es and internal bodily feelings
very poor emotional reactivity. suggested a more general emo-
The marked neuropsychological tional anaesthesia and/or a
decits were a moderate proso- decient means of expression. It is
pagnosia and severely disordered possible that a limbic component
recognition of facial emotions, might be involved, thus making
gender and age. Expressive facial affective appreciation also de-
emotion, whole body psychomo- cient.
C. Njiokiktjien (&) A. Verschoor tor expression and speech proso-
L. de Sonneville V. Op het Veld dy were quasi absent as well. In all j Key words Asperger's syn-
N. Toorenaar
Pediatric outpatients clinic three boys these facial processing drome autism facial emotion
Free University Hospital decits were more or less isolated, right hemisphere decit
P.O. Box 7057 and general visuospatial func-
NL-1007 MB Amsterdam tions, attention, formal language j Abbreviations AS Asperger's
The Netherlands
and scholastic performances were syndrome; B, C, D abbreviation for
C. Njiokiktjien A. Verschoor C. Huyser normal or even highly developed subjects described; ANT Amster-
Triversum with the exception of decient dam Neuropsychological Test;
Institute for child and adolescent
psychiatry
gestalt perception in B. We con- RH Right Hemisphere; LH Left
K.Boekestraat 5 sider the decient facial emotion Hemisphere; PIQ Performance IQ;
1817 EZ Alkmaar, The Netherlands perception as an important VIQ Verbal IQ

denition of autistic behaviour the clinical core of


Introduction autism is `decient or absent social relatedness'.
When performing a study with autistic children one However, this denition neither resolves the ques-
ECAP 0204

has to clarify what one's position is regarding the tion whether autism is based on one single or on
essence of autism. In our opinion, a sound clinical several partial decits, nor answers what the
80 European Child & Adolescent Psychiatry, Vol. 10, No. 1 (2001)
Steinkopff Verlag 2001

pathophysiologic mechanism(s) is (are). Being in- Assessment methods


terested in the neuropsychological background of
abnormal contact, we asked ourselves whether there j Clinical examinations
are agnosias pertaining to various aspects of the
non-verbal or body language. Langdell (28) pointed History, psychiatric examination (by child psychia-
to facial identity recognition problems and Hob- trist CH) and neurological examination and clinical
son's initial studies showed that autistic children neuropsychological screening (by pediatric neurolo-
are impaired in the ability to link appropriately gist CN).
drawn and photographed faces with videotaped
emotional gestures and voices (23), to link drawn
gestures with faces on video (24) and also faces j Neuropsychological examination
with voices (26). Weeks and Hobson (53) clearly (by neuropsychologists CAV and NT)
stated that autistic children tend to be insensitive Sensory Integration and Praxis tests (B)
to other people's facial expression of emotions. Dutch version of the WISC-R (boys B, C, D), WISC
Tantam et al. (47) subsequently conrmed that III (B)
autists have difculties in distinguishing between Woodcock Johnson test of cognitive ability (B)
facial expressions and in naming them. Macdonald Kaufman ABC; Gestalt closure and Spatial Locali-
et al. (30) also stressed the disturbed expression of sation (C, D)
emotions in autists and Yirmiya et al. (56) drew Peabody Picture Vocabulary Test (B)
attention to the at/neutral or ambiguous facial TVK Dutch language Test for Children; Active and
expression. passive vocabulary (C, D)
Anamnestic data and observation of three high Beery VMI (B, C, D)
functioning boys (B, C and D), diagnosed as Asperger
autists according to DSM-IV criteria (3), suggested a
severe lack of comprehension of emotions in other j Recognition of smells
people. This led us to perform an extensive examin-
ation, including a set of computerised tests developed Ten common substances in containers have to be
to evaluate speed and accuracy of processing facial identied by matching them to a written list of 15
emotion information. substance names. The substances are known to the
Asperger's syndrome (AS) is known as a develop- subject.
mental disorder in the autism spectrum. The syn-
drome is not only accepted as a mild subtype of
autism (20, 45, 46, 54), but there is an argument to j Photo screening tasks
retain the name Asperger's syndrome because AS is a
clinical entity with specic characteristics, among 1) Discrimination of gender and age. The subject has
others a better prognosis and a higher prevalence rate to successively identify pictures of boys, girls, men
than autism with more severe verbal components and women that have been printed on a card in
(17, 34). We take the position that AS is a subtype of random order,
autism in high functioning people. The clinical 2) Identication of the basic emotions `happiness',
symptoms of AS include abnormal social relatedness `sadness', `anger', and `fear' from a card with
and a restricted range of behaviours and interests, and pictures of adult men and women displaying the
exclude marked formal spoken language disorders four emotions. The subject has to successively
and other signicant cognitive decits and neuropsy- point out the respective emotions.
chiatric disorders. Throughout the literature there are
small differences depending on whether one looks at
j Computerised tasks selected from the Amsterdam
the work of individual authors (17, 45, 46), or at
Neuropsychological Tasks battery [ANT, de Sonneville,
diagnostic criteria in DSM-IV (3) or ICD-10 (55). For
1999 (15, 16)]
example clumsiness is included in ICD-10, but
excluded in DSM-IV. 1. The rst four tasks are `control' tasks: they provide
The boys B, C and D have, in this order, symptoms a reference with regard to the performance in the
with a decreasing clinical severity. B will be described facial emotion tasks, on the following levels
extensively because he showed added symptoms respectively:
which are interesting for the discussion on the  Baseline Speed: to measure simple reaction time
processing of emotions; the two other boys with (detection of stimulus presence).
essentially the same facial processing decits are  Sustained Attention (attention capacity): in this
presented in brief. task, 50 series of 12 dot patterns are presented in
C. Njiokiktjien et al. 81
Disordered recognition of facial emotions

continuous succession. Subjects have to discrim- j Family


inate between patterns with three, four and ve
dots. Evaluation parameters are tempo, tempo Both parents have an academic background and live
uctuation and accuracy. separately. The brother of the father, as well as an
 Feature Identication: to evaluate speed and older brother of B, attended university before the age
accuracy of processing abstract visuospatial of 16 to study physics and chemistry. Neither of them
patterns (non-facial information). The subject were autistic.
has to detect a specic conguration of red and
white blocks (target) which may, or may not, be
present in a signal which always consists of four j Perinatal history and early development
patterns. The constituting patterns may look
very similar to the target, which makes target B is a second child. Pregnancy was accompanied by
detection hard, or may look very dissimilar to hyperemesis and medication for unspecied non-
the target, which makes target detection easy. gynaecological infections. He was prematurely born
 Face Recognition: to investigate speed and at 31 weeks in breech position, birthweight 1765 g, and
accuracy of recognising a neutral face. Each nursed for 2 weeks in an incubator with no complica-
signal is preceded by a probe (the to be identied tions other than polycythemia. B was very hypotonic
face), and consists of a random set of four faces with a head lag. Sitting independently as well as walking
of the same age and gender that are selected from occurred only after 15 to 17 months. Eye contact
a stimulus set of digitised photographs of 20 was established very early. The behaviour problems
different people (boys, girls, men, women). The became obvious from the age of 4 years onwards.
subject has to detect the probe which may, or
may not, be present in the signal.
j Speech and language
2. Identication of Facial Expressions: to investigate
speed and accuracy of processing facial expres-
Normal milestones. The family is bilingual (Hebrew
sions (emotions). The signal consists of one
and Dutch). B speaks three languages: Hebrew,
(digitised) photograph of a face which may show
English which he learnt from his father's side before
any of the following expressions: happiness, sad-
the age of 3 years 6 months and in an international
ness, anger, fear, disgust, surprise, shame, con-
school, and Dutch since the age of 3 years 6 months.
tempt. The stimulus set consists of pictures of four
He understands jokes, although he sometimes takes
different people (two men, two women) who all
things literally. Verbalisation is slow, especially `on
show these expressions. The task consists of four
command' and in subjects outside his domain of
parts in which the target expression (the to be
interests. B speaks without prosodic intonation and
identied emotion) is happiness, sadness, anger,
one never hears any excitement expressed although
fear, respectively.
sometimes irritation.
3. Matching of Facial Expressions: in contrast with the
identication task, the subject needs not identify a
certain facial expression but is asked to judge j Scholastic performances
whether two faces show the same or a different
expression. The signal consists of a pair of pictures, Reading was acquired ``by himself'' before the age of
always of different people, from the same stimulus 6 years in three languages. Spelling is average,
set as is used in the identication task. handwriting is slow but neat. At the age of 10 years
his mathematical abilities and understanding of
subjects in mathematics and physics were at an
Case description of B advanced college level. His interests, narrow though
not bizarre, are rooted in his high giftedness.
j Reason for referral

B, a boy aged 10 years 6 months, was referred for j Facial behaviour


social contact problems which were so severe that he
had been removed from his school (see social Eye contact is normal at home only. Facial expression
behaviour in History). In addition, B, a right-hander, is very impassive and he does not show affect, only
had mild hand motor problems and as a much occasionally happiness. He does not react to the facial
younger child had been clumsy with gross body emotions of others. A smile is identied ``because the
movements. One year before referral B had tempo- edges of the mouth go upwards''. B often fails to
rarily slight tic symptoms. recognise people who are familiar to him.
82 European Child & Adolescent Psychiatry, Vol. 10, No. 1 (2001)
Steinkopff Verlag 2001

j Social behaviour further abnormalities in posture and motor behaviour.


At rst contact he was willing to co-operate but seemed
B does adapt to changes and requirements from others almost unaware of the social interaction. He did not
such as the school teacher but only if these are initiate or respond to formal greetings, and personal
acceptable to him through logical understanding. This questions and eye contact were often avoided. During
often leads to refusal. B needs a long time to adapt to the testing period there was little sense of rapport
strangers. He does not initiate the making of contact building with the examiners, and any contact that was
and instead waits for others to make an approach. made seemed to vanish at the end of the session. He
Once a relationship is established, it is frequently did not recognise the neurologist whom he had met
temporary and often breaks down. He appears to lack 6 weeks previously. He often had the tendency to
assertion and never displays fear or anger. With one control the conversation, to set it on his own terms and
friend B talks a lot about his interests which are to focus on areas of personal interest, these being
physics, mathematics and computers. B does not like physics and computers. Interest and involvement in
phone calls. Impulsiveness, hyperactivity, distractibil- the tests was dominated by these strong preferences.
ity, sensation seeking, tactile defensiveness and affec- In performing tasks, in which he could excel, B was
tive instability are all absent. very eager, swift and concentrated, and showed pride
According to anamnestic data, B's emotions and in his good results. When confronted with a task
feelings could be classied according to their degree of which he could not readily solve, he was often
presence and intensity (Table 1). The emotions which obstructive. He would reside in silence and simply
are present tend to be positive ones while negative not respond, being very reluctant to try and guess. In
emotions are absent. Absent means that they are never these subject areas, thinking seemed slow and rigid.
or rarely expressed by B himself and/or that he
never shows recognition of these emotions in others.
j Psychiatric examination

Assessment results in B B did not want to play and he asked the reason for
every part of the examination. Conversation and
j Clinical examinations: appearance and behaviour personal wishes were restricted to his interests.
(an impression shared by all examiners) Thinking appeared to be rigid and concrete, and he
spoke of having complete control over his fantasy life.
B is a pleasant-looking, slender boy who is restless and In conclusion, B has a severe pervasive disorder of the
ill at ease. He has a rather impassive facial and body Asperger type (DSM-IV, axis I), with an island of
expression and speaks slowly with a squeaky tone and extreme well functioning. In social and emotional
strange prosody. The content of his speech is formal development he is lagging far behind. He has no other
and pedantic. Apart from an `open mouth' tendency psychiatric symptoms, syndromes or disorders. Fur-
and an inexpressive whole body behaviour there are no ther DSM-IV classication: axis II: no diagnosis; axis

Table 1 Presence and intensity of emotions and feelings in B

1. Present emotions, but without nuance


 Happiness, love, satisfaction; likes cuddling before sleep;
 Interest, self-confidence, pride;
 Humour, mostly verbal. B does not like slapstick humour. He understands sarcasm and can pretend it, but without prosody;
 Interest in the difference between beautiful and ugly and a taste for clothes, surroundings and music.
B knows how to play the violin and the piano, but does not like it. He prefers the computer;
 Irritation, boredom, anger.
2. Absent emotions or feelings
 Hope, expectation, compassion, patience;
 Amazement, astonishment;
 Excitement, fear, panic;
 Sadness, loneliness, depressed feelings, despair;
 Shame, stress, self-consciousness;
 Hate;
 Fear of concrete events; curiosity, frustration and deception are barely felt and rarely displayed.
3. Absent or weak body sensations
 Pain, hunger, nausea, absence of well-being during illnesses. B probably does not experience these sensations adequately, and/or does
not react to them with any emotion. He once said: ``Apparently I bumped my head, because I can feel a lump with my hand'';
 No reaction to loud noises;
 Unable to recognise smell; deviant taste and eating habits, preference for carbohydrates.
C. Njiokiktjien et al. 83
Disordered recognition of facial emotions

III: anosmic e.c.i.; axis IV: problems with the social of object use was very hesitant. This task is used as an
environment, school problems, one-parent family. assessment of ideomotor praxis; the subject has to
show how to use, for example, a toothbrush. Sometimes
B was unable to respond at all. Bilateral integration and
j Neurological examination/basic neuromotor
co-ordination were normal. Basic eye-hand co-ordina-
functions
tion scores in a line following task were below average
for the right hand, and average for the left hand.
Head circumference 53 cm. Slight lordosis, at feet
Graphic praxis in copying gures was good, the VMI
and hypotonia, including the oral area; asymmetrical
score was well above age level. Drawing a person from
and symmetrical tonic neck reex were still present;
memory was very difcult, B needed an example. Hand-
standing balance on one leg was difcult on the right
writing was neat but slow, the pencil grip was tense.
side. Irregular hand motor movements while per-
forming pronation/supination and open/close hands
according to Touwen's manual (48). Bimanual alter- j Speech and language
nate movements and axial movements were also
poorly executed. Speech was slow and mildly inarticulate. Prosody was
nearly absent, sometimes even bizarre. During narra-
j Sensory awareness, perception and gnosis tion he was dysuent with word-nding difculties,
sound, word, and phrase repetitions as well as sound
 Acoustic. Anamnestic data showing a general additions and prolongations in Dutch and English.
hyposensitivity were conrmed; B did not react to Dysuency was especially apparent when B had to
loud and bothering noises. describe social situations and events. He was, howev-
 Smell. B was anosmic, he could not recognise one of er, more uent when the subjects were physics or
ten common substances and could only indicate the computers. On the Peabody PV Test in English, his
existence and intensity of a smell. When asked for passive vocabulary was below average and his ex-
his appraisal he referred to his quick withdrawal pressive vocabulary was well below his age level.
from the vinegar container saying ``my reaction Syntactic structures in his spontaneous speech were
must have meant that I did not like it''. age-appropriate. Tests on these abilities were not
 Somatosensory perception. Kinaesthesia and tactile performed in Dutch and Hebrew.
perception were normal but signicantly less
adequate on the right side. Right-left orientation
j Intelligence
was normal. From his history it was known that his
reactions to pain were slow or absent.
At 8 years 8 months, the formal IQ scores in the Dutch
 Visual and auditory perception. B had an above
WISC-R were at an average level. However, these
average score in a test of gure-ground perception,
scores were not representative of B's capacities as his
and an average score in a visual matching task.
rigidity and selective co-operation made it impossible
However, he had very low scores in visual and
for the examiner to arrive at a valid interpretation. The
auditory closure tasks. Although these closure tasks
subtest prole was very erratic, standard scores
were administered in English and word retrieval
varying between 5 and 19. Nine months later the
difculties could have inuenced the performance,
American WISC-III was administered. Rapport and
the extremely low level was taken to indicate a
co-operation were better, but the results were more or
decient gestalt perception.
less the same. After having taken into account that B is
not a native English speaker, together with a possible
j Praxis learning effect from using the same test after a short
time interval, the examiner judged the results to
B is a right-hander. Gnosopraxis was poor in two accurately reect current functioning.
different tests for imitation of postures. Representation B's performance showed the following results:

Information 6 Picture Completion 10 IQ Factor scores


Similarities 12 Codes 14 Full scale: 115 Verbal Comprehension 90
Arithmetic 19 Picture Arrangement 6 Verbal: 110 Perceptual Organisation 110
Vocabulary 9 Block Design 17 Perform 120 Freedom from Distraction 145
Comprehension 6 Object Assembly 15 Processing Speed 125
Digit Span 17 Mazes 19
Symbol Search 14
84 European Child & Adolescent Psychiatry, Vol. 10, No. 1 (2001)
Steinkopff Verlag 2001

In general, the subtest and factor score prole were


again extremely erratic. The low scores in the verbal
subtests Information and Comprehension, seemed,
apart from verbal uency problems, to reect his
problems in social knowledge and pragmatic reason-
ing. This was again seen in his performance in the
Picture Arrangement subtest and to a lesser degree in
both the Vocabulary and Picture Completion tests. In
the subtest Similarities these problems could be
surpassed by good abstract logic reasoning and
although arithmetic was tested in the verbal realm,
B showed an excellent ability. The high scores in the
performance subtests Block Design and Object As-
sembly showed his extremely well-developed visual
analysis, synthesis and non-verbal abstract reasoning
skills.
Fig. 1 Task performance of B in z-scores as a function of task and signal type
(10 yrs 6 mo) As regards baseline speed, separate bars have been plotted to
j Memory indicate B's reaction time and his fluctuation in speed. For the sustained
attention task, 3 bars indicate B's tempo, fluctuation in tempo, and mean
Short-term memory for non-verbal auditory sequences accuracy respectively. For the remaining tasks, per type of signal the pairs of
(Stambak's rhythm reproduction) was normal. Mem- bars indicate the speed and accuracy of responses. Z-score values lower than
)4 have been printed in the graph
ory for verbal sequences (digits, words and sentences)
was very accurate. Associative learning with a social
connotation, like in Memory for Names from the WJR- good basic speed, tempo and accuracy in sustained
COG, was again very poor. Long term memory, as can attention and visuo-spatial analysis.
be determined from, for example, the level of factual
knowledge on the WISC subtest Information, seemed
to be strongly inuenced by B's preferences. He was j Processing of neutral facial information (age,
unable to name the different seasons or tell the word gender, prosopognosis) (Fig. 1)
used for a young cow, but he could explain how to make
uid out of a gas and could describe the causes of an In the picture screening task B could only discrim-
eclipse of the sun. inate between gender and age with great difculty.
The recognition of females and adults proved more
difcult for him than the recognition of males and
j Planning and cognitive flexibility children. RT scores in the ANT facial recognition task
were far below average and accuracy was below
Planning skills were excellent on the WISC subtest average especially with non-targets: B scored many
Mazes test. Performance on simple go-no-go tasks false alarms, i.e. erroneously deciding that the probe
was normal. Further formal testing in this area could face was present in the signal.
not be done due to circumstances. There was a
denite element of overfocused attention and thought
rigidity could be observed in the difcult social area. j Processing of emotional facial information (Fig. 1)
However, a high performance in maths and physics
would also normally involve a exibility in problem At the rst attempt to administer the picture screen-
solving. ing task, B did not respond at all. At the second
attempt, some weeks later, he could identify the
pictures of the happy faces fairly quickly, commenting
j Attention and processing of non-facial that he could distinguish them by the mouth. Only
information (Fig. 1) with extreme reluctance and after extensive descrip-
tion of the `key features' of an angry face was he able
Baseline speed and stability, as well as tempo, to identify one of the two pictures of an angry
uctuation in tempo and accuracy in sustained expression. When asked to make an angry face
attention were in the above average or high average himself he said he was unable to imagine his own
range. The same was true for his performance in the anger. Furthermore, he could not be persuaded to
Feature Identication task. In summary, B showed identify the other expressions of fear and sadness. In
C. Njiokiktjien et al. 85
Disordered recognition of facial emotions

the ANT task `identication of emotion' with happy as problems and particularly marked problems in social
the target emotion, he was only able to make positive contact. They relate poorly to other people in general,
identications with appropriate speed and accuracy seldom play with age mates and appear particularly
(deciding that the face looks happy when the signal unaware and unresponsive to their own emotions.
indeed shows a happy face). Negative identication They have exclusive interests in non-social areas such
(rejection of signals exhibiting non-happy faces) were as space ships and computers, and are characterised
reasonably accurate but extremely slow. Speed of as inexible, unimaginative and pedantic. Regarding
processing when the identication of `angry' expres- non-verbal behaviour, eye contact is poor and facial
sions was required was very slow but accurate. Again, expression is impassive. They have trouble interpret-
the target emotions of `fear' and `sadness' could not ing body language and prosody in others. In both
be administered because he refused to respond. boys formal speech and language development is
Finally, when asked to match facial emotions, B's normal and scholastic learning presents no problems.
performance showed a below-average overall score in In both families the parents are divorced and there
processing similar emotion pairs and in processing are social contact disorders in rst degree relatives on
dissimilar emotion pairs. Both overall scores were the father's side.
favourably inuenced by his reasonable level of Boy C had a normal perinatal history; he is,
processing pairs containing at least one happy face. however, clumsy, has vocal and motor tics and can
Signalling pairs of angry faces was accurate but slow, further be described as restless, impulsive and
identifying pairs of sad faces was practically impos- oppositional with strong reactive aggression. He was
sible, and identication of frightened faces was unable to function socially at a regular school. A
inaccurate and extremely slow. previous psychiatric examination referred to his
In summary, B has no major neurological signs, behaviour as an oppositional deant disorder, which
but basic neuromotor functions are immature and was later interpreted as an AS type autistic disorder.
there is hypotonia. There is a dyspraxia and B has Boy D was born ve weeks preterm but without
ideomotor praxis representation problems. Further- further complications. Apart from two febrile con-
more, he exhibits acoustic hyposensitivity, anosmia vulsions he has had no medical problems. He has
and visual and auditory Gestalt perception decien- normal motor skills and still attends a regular
cies. Kallman's syndrome was excluded. Speech and school.
language reveal dysprosody and dysuency, especially After psychiatric, neurological and neuropsycho-
within the social realm but this was not formally logical examination both boys were diagnosed as high
assessed in his rst (Hebrew) and second language functioning with AS. Dyspraxia, tics and compulsive
(Dutch). The IQ prole is extremely erratic: visuospa- behaviour are a comorbidity in boy C only. There
tial analysis, abstract logical reasoning, planning and were no prominent neurological signs, only some
short term memory without social connotations are minor neuromotor dysfunctions in boy C.
all good to excellent. B's performance was very Both boys are right-handed. Formal intelligence is
decient in a number of facial perception tests, well above average but performance IQ is signicantly
neutral as well as emotional, and this cannot be lower than verbal IQ. Nonetheless most test results,
explained by decient general information processing including those pertaining to visual memory for non-
speed, sustained attention or visuospatial analysis. facial information and visual gestalt perception, fall
There is a strong indication that B tries to use his within normal limits.
good visuospatial analysis and formal cognitive The computerised reaction time tests (Figs. 2 and
reasoning skills in the perception and interpretation 3) show baseline speed, tempo and accuracy in
of the facial gestalts with the personal features and sustained attention and visuospatial analysis tasks to
emotional information. By selecting one salient part be fundamentally normal. On the other hand, results
of an expression, e.g. the open mouth and visible teeth in many aspects of the face and facial expression
in the happy face, he could succeed in identifying this identication tasks are clearly below average. In the
expression. All other facial emotions are far too face recognition task, both boys display slow and
complex and diverse in their expressions, as are the inaccurate non target responses (target face absent)
neutral facial characteristics, to be correctly perceived reecting an insufcient internal representation or
by analysis. active memory for faces. In the identication of facial
expression task boy C is predominantly slow, but he
can identify what the face depicts, while boy D is
Case description of C and D extremely inaccurate as well as being slow. In the
matching of facial expressions both boys are slow and
Two boys, C and D aged 6 years 7 months and 8 years inaccurate, boy C having particular trouble deciding
3 months respectively were referred for behaviour whether the faces show the same expression, and boy
86 European Child & Adolescent Psychiatry, Vol. 10, No. 1 (2001)
Steinkopff Verlag 2001

of emotions in the face, the voice and the body, the


most marked symptom being a facial recognition
decit.
1. Facial contact: all three boys have an impassive
facial expression. We could detect a quasi-absent
understanding of negative facial emotions in B,
which was less marked in C and D. Moreover there
was a signicantly decient judgement of facial age
and gender, less marked in C and D. Prosopagnosia
was clinically present in B, in C and D in a covert
way only (see also Ref. 9). This symptom might be
partly due to an obvious lack of interest in other
people, thus resulting in no imprinting. All three
boys avoided eye contact, and gaze avoidance was
even displayed towards the computer screen during
the tests with faces. Faces, regardless of the form of
Fig. 2 Task performance of C in z-scores as a function of task and signal type presentation, appear to perplex them. Among the
(8 yrs 3 mo). For legends see Fig. 1 various face processing decits in the subjects
under study, the emotional expression and percep-
tion seem most marked (7).
2. B has a dysprosody, and his voice is monotonous,
in C and D this is less obvious. A receptive
dysprosody was present in the three boys in
anamnestic data. The testing of receptive dyspro-
sody remains beyond this discussion.
3. B has very inexpressive body movements and he
shows no affect with his body. It could not be
assessed whether he was able to judge expressive
body movements in other people. In C and D this
expressive symptom was less marked.
One may consider the facial affect recognition de-
ciency in the three boys as a common core symptom
and the other face processing dysfunctions (facial
identity, gender and age processing) as important co-
morbid conditions, not necessarily occurring in AS,
respectively autism. It is well known that these three
Fig. 3 Task performance of D in z-scores as a function of task and signal type functions are separately represented in the brain
(6 yrs 7 mo). For legends see Fig. 1
(1, 2, 18, 49, 35), obeying the double dissociation rule
in patients. The same is true for body language, speech
D tending to erroneously decide that different prosody and object recognition. One may even state
expressions are the same. that, although expression suffers from abnormal
In conclusion, both boys show a marked receptive reception, expressive and receptive functions are
facial emotion processing dysfunction alongside in- separated. This is true for formal spoken language,
adequate face identication skills, but there is no for prosody and probably for the processing of various
overt prosopagnosia. aspects of facial information as well.

Discussion j Emotion processing deficits in the subjects


under study suggest a partial right hemisphere (RH)
j Emotion processing deficits in the subjects or bilateral dysfunction
under study are present in several modalities
One may rst question whether the dysfunctions within
Although the literature often focuses only on the face, the three domains have one pathogenetic locus or
anamnestic data as well as assessment suggest an neural circuit and why they cluster. As children engage
inadequate comprehension and a decient expression in emotion recognition tasks there are hemispheric
C. Njiokiktjien et al. 87
Disordered recognition of facial emotions

electrophysiological differences, depending on what B also had right-sided sensory and motor distur-
the child is expecting from the task (12). Although they bances, presumably on the basis of LH dysfunction by
are doubly dissociated, it is generally assumed that perinatal damage. It is not excluded that this LH
facial, body and emotional voice perception are mainly damage also contributes to B's autistic features.
controlled by the RH (8, 39, 40). However, left hemi- Perinatal insults in AS are mentioned by Gillberg
sphere (LH) participation, especially connected to (19) as a frequently occurring aetiological factor. In B,
verbal labelling (44), is not excluded (29, 35). It is also because of refusal, we could not perform brain neuro-
the case that some people adhere to the `valence imaging and EEG to nd out more about the
hypothesis', i.e. the idea that the LH harbours more pathogenesis. In C and D there is familial occurrence
positive emotions, the RH more negative emotions of contact disorders. In these boys, with a less severe
(31). However, a number of studies (8, 29, 35) do not clinical picture, there is no other sign of perinatal
support this hypothesis. In general, it has been rightly brain damage. This, therefore, suggests that the
argued that emotion perception decits are predomi- aetiological dimension might be the reason for a
nantly due to developmental RH dysfunction (32). different clinical picture.
One may also approach the question from the angle
of well-known RH syndromes. Rourke's (41) so-called
non-verbal learning disabilities (NLD) syndrome, j The significance of receptive and expressive
associated with RH dysfunction, often includes marked facial processing abnormalities in autists
social interaction problems. Many clinical features,
encompassed in the NLD syndrome, are also found in Our study revealed the presence of facial processing
what has been described by others as the developmental abnormalities, for the rst time, in reaction time tasks,
learning disabilities of the RH or RH decit syndrome, which enhances the sensitivity of deviant ndings. Such
including abnormal interpretation and expression of abnormalities were rst proposed by Langdell (28),
affect (a.o. 50, 51). Klin et al. (27), arguing that AS and then by Weeks and Hobson (53) and Tantam et al. (47)
the NLD syndrome converge, found the performance specically in AS, whereas Macdonald et al. (30) and
IQ (PIQ) to be lower than the verbal IQ (VIQ) in their Yirmiya et al. (56) stressed abnormal facial expressions
AS group, which does not mean, however, that all (see introduction). In one study the presence of specic
children with low PIQ have AS. Irregular cognitive decits in the perception of faces per se was denied,
proles with a low PIQ can point to less optimal RH because autists have no obvious problem in assembling
function. However, many children with RH symptoms puzzles of photographs of human faces (52). This could
and relatively low PIQs are not diagnosed as being be explained by the piece by piece approach and inner
autists. In a sample of 45 children with low PIQ and language reasoning of autists. Another study (11)
higher VIQ and a discrepancy of at least 25 points we suggested a general perceptual decit, not specic to
have only diagnosed eight mildly autistic children (33). faces or emotions. Hobson's ndings (see also an
Moreover, a low PIQ does not gure in the ICD-10 overview by Hobson, 25) were found to be inconclusive
criteria for AS, neither is a low PIQ a sine qua non for in other studies and Ozonoff et al. (34) have rightly
the NLD syndrome (41). Our patients C and D had a suggested that multiple primary decits underly autis-
lower PIQ than VIQ. Although B had a lower VIQ than tic behaviour. Thus, as Davies et al. (11) state, group
PIQ, he has been described by the psychologists as averages mask substantial individual variation. Weak
verbally intelligent with excellent attention and nu- statistical effects might also be explained as a large
merical abilities. He had low vocabulary, information overlap in distributions (6). Our results demonstrate
and comprehension scores on the WISC for three that some autists are able to perform in the receptive
reasons: trilinguism, no interest in social aspects, and domain while others are less able to perform. If one
near-mutistic behaviour as soon as questions con- takes these neuropsychological facts into account, one
cerned social areas. When questioned about his may propose that autism is concurrent with an
inability to name the seasons in English, he answered underlying spectrum of neuropsychological decits of
logically: ``I do not need to know them because in varying severity. Whether one regards the limitations
Hebrew the language spoken at home you can name of the face, the whole body or the prosody to be
them by season 1, 2, 3 and 4.'' This answer also shows responsible for the decient social engagement, is more
B's `logico-affective state' (see further), which may or less arbitrary. However, the effects of face and voice
impoverish his formal VIQ. deciencies commence from birth onwards, whereas
The combination of the above-mentioned dysfunc- the consequences of body language deciencies are
tions regarding emotions in the face, body and manifest later. We suspect, however, that abnormal
voice might have an aetiological background in B, receptive processing of face, voice and body language
namely diffuse perinatal damage, sparing other RH may have an additive effect on the construction of the
functions and most LH language functions. affective world of a child. It is well known from other
88 European Child & Adolescent Psychiatry, Vol. 10, No. 1 (2001)
Steinkopff Verlag 2001

developmental disorders, for example the dysphasias, had a normal visuospatial function. `Clumsiness'
that receptive disorders have a deleterious inuence on might also infer poor overall body language. The
language function and a worse prognosis. B is an `clumsy' imitation of postures by B and C, due to
example of a boy with severe receptive and expressive dyspraxia, might indicate a special difculty experi-
emotion function disturbances. The overall clinical enced by autists in understanding other people's
picture is less severe in C and D. perspectives (43). Dyspraxia and hypotonia are not
The literature might lead one to question whether specic markers in autists if one looks at the results of
deviant perceptual facial processing is the underlying a large study by Rapin and collaborators (38). In B
key factor, whether this dysfunction is always based and C drawing and pretending ideomotor acts on
on the same mechanism and whether this is the only request were poor (clumsily and hesitantly executed),
pathogenetic factor underlying the decient social as was imaginative play at pre-school age (in B, C and
relatedness in autism. We suggest that the underlying D). This might reect a poor visual imagery function.
abnormal processing of affect may be crucial in In the WISC-R `Comprehension' difculties (prag-
explaining the social behaviour of some autistic matic reasoning) might also be due to imagination
children. We would not propose, however, that this problems (21). Visual mental imagery is a function of
is the only pathogenetic mechanism or that this the visual association cortex and asymmetrically
mechanism always has an identical structure. lateralised to the left (14), whereas there is no
hemispheric lateralisation when mental rotation is
involved (10). An alternative explanatory concept for
j Co-morbid symptoms defective visual imagery might be poor `conservation'
(57).
A range of stimuli other than facial, bodily and vocal Overfocused attention and mental set rigidity (in B,
provoked an abnormal reaction in B. His insensitivity C and D), observed during psychological evaluation,
to pain, smells, noises and internal bodily feelings might both be due to executive dysfunction, possibly
suggest a more general emotional anaesthesia. Hypo- a RH symptom.
emotionality of visually observed events has been In B, his absence of self-consciousness and lack of
interpreted as a visual-limbic disconnection (5). Facial, insight of his own desires and emotions can be seen as
bodily and voiced emotional signals as well as pain, reliable anamnestic data and might point to some
smells etc. might have a common neural target in the kind of neglect or anosognosia, a RH symptom.
limbic system (Papez' circuit) where these signals Hermelin and O'Connor (22) have proposed the
already cortically recognised provoke an emotional notion of a ``logico-affective state'' in high functioning
resonance in order to be memorised and transferred to autists when part of the emotional problems are
the hypothalamic regions for autonomic expression, overcome by using cognitive or intellectual strategies.
and via the thalamus to the prefrontal cortex for This might be the case in B and C. While interpreting
expression. In children with autistic regression, limbic faces or situations they often employed reasoning or
pathology (notably of the amygdala) has been shown they used gestural or environmental cues. It is as if B
(13). Facial fear perception involves the amygdala used his mathematical talents when taking decisions
without lateralisation in a fMRI study (4, 37) and facial and he only seemed motivated by logical insights.
disgust activates the anterior insular cortex (37), which Gestalt perception was decient (in B), but visuo-
is also involved in responses to offensive tastes (36). A spatial and gure-back-ground perceptual functions
study by Borod et al. (8) supports not only the RH were normal or even highly developed (in B, C and D).
hypothesis for identication of emotion across multi- While interpreting faces B often looked at facial
ple channels, but also the existence of a single details, a `piecemeal' approach, using no holistic
processor across these channels. This might be the strategy. This has also been noted by Weeks and
superior temporal gyrus (37). B's problems in express- Hobson (53). This simultanagnosia a RH symptom
ing feelings in general, not only socially driven feelings, was also present when interpreting non-facial
might be due to the inadequate working of a common objects. B's and C's relatively high performance in
neural limbic and/or prefrontal circuit. This does, block design suggest a propensity for the use of
alternatively, not exclude a possible thalamic dysfunc- details instead of the normal Gestalt processing of
tion. patterns. This occurs in many children with mild
Motor clumsiness has been forwarded as an autism and AS, and has been called `low central
integral symptom in AS (19, 55). When one refers to coherence' (42). The high `digit span' in B (above
this term at the elementary manual level, present in B average in C and D) as well as `block design'
and C, we consider it as aspecic co-morbidity. Some performance are explained in the same way (21).
people use the term `clumsiness' to describe dyspr- High `block design' performances are not explained
axia, again an aspecic co-morbid condition in B, who by high visuospatial insight (21, 42).
C. Njiokiktjien et al. 89
Disordered recognition of facial emotions

Conclusion absent social relatedness and might also be related to


other problems in autists.
B, and in a less severe degree C and D are AS type In our opinion, facial, body and voice recognition,
autistic boys with severe receptive and expressive processed at different cortical levels, might converge
emotional function disturbances in three areas of towards an underlying common locus in the limbic
non-verbal social contact: face, body and voice. We system for affective appreciation. A more general
consider the absence of emotion perception as a emotional anaesthesia and/or expression disturbance
crucial pathogenetic factor for the autistic behaviour beyond the social domain is thus a possibility. The
and this clinical picture seems to be rooted in a RH or perceptual (cortical and possibly thalamic) and/or
bilateral decit. The poor age and gender identica- appreciation dysfunctions (limbic) have a deleterious
tion and the partial prosopagnosia are facial process- additive impact on emerging emotion concepts. This
ing disorders that are not necessarily present in all does not exclude rather isolated expressive, not
autists with facial emotion perception problems. receptive, dysfunctions in other autists, explaining
Mental rigidity, poor visual mental imagery and the variance of ndings in larger groups of autists.
imagery of other people's perspective as well as The aetiological background in B might be perinatal
pragmatic language aspects contribute to absent damage, sparing other RH functions and major
social relatedness as well, while the dysphasic symp- language functions, while genetic factors play a role
toms as well as most motor symptoms are aspecic in C and D.
co-morbidity. Ritualism and bizarre or narrow inter- j Acknowledgements This research project has been supported by
ests are possibly more a consequence than a cause of grant 28-2915 of Zorgonderzoek Nederland (Praeventiefonds).

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