The Mesial-temporal Lobe and Autism: Case Report and Review Alexander H . Hoon, Jr. Allan L . Reiss
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Autism is the prototypal disorder in the class of neuropsychiatric diseases known as pervasive developmental disorders. The behavioral syndrome of autism consists of significant abnormalities in social interaction, behavior and communication. Mental retardation is usual, but not invariable. Despite research on human and animal models, little is known of the specific neurobiological factors directly responsible for the pathogenesis of autism. Autism has been associated with a number of medical conditions, including congenital rubella, herpes encephalitis, fragile-x syndrome, tuberous sclerosis, neurofibromatosis and phenylketonuria (Chess 1971, Reiss ef al. 1986). Neuropathological and brain-imaging abnormalities in cases with and without presumed biological etiology have led to neurophysiological hypotheses linking dysfunction of various areas of the brain t o autism. These areas include the temporal lobe (Damasio and Maurer 1978), cerebellum (Courchesne ef al. 1988) and brainstem (Ornitz 1985).
In this case report we describe a young male child with a left temporal oligodendroglioma, who demonstrated a constellation of autistic behaviors meeting DSMI l l - R criteria for pervasive developmental 252
disorder. Some of these a u t i s t i c symptoms
resolved after resection, while other qualitative signs of developmental abnormality emerged or persisted. Given reports of human neuropathology and animal models indicating an association between temporal lobe lesions and autism, we believe that the tumor disrupted normal neurodevelopment, resulting in a clinical picture which included autistic behavior. Clinical and neuro-anatomical features of this case are presented to add to the understanding of the neurobiological basis of autistic behavior.
Case report J.T. was born to a 32-year-old gravida 2 woman. Pregnancy was complicated by symptomatically managed ulcerative colitis, for which she look prednisone during the first six weeks of pregnancy. Fetal activity was described as normal in onset and quality. There were no infections or exposure to teratogens. Weight gain was I I .35kg. He was delivered at 39 weeks gestation, with birthweight and head circumference at the 60th and 75th centiles, respectively. Although there were mild signs of fetal distress at delivery, no resuscitation was required. He was discharged h o m c on t h e second post-partum day. A head CT scan was performed at six weeks of age because of rapid increase in head circumference to the 95th centile. The results were interpreted as normal at that time, although retrospective evaluation of this scan suggested abnormalities (discussed below). There was no subsequent abnormal increase in head size.
s-52
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TABLE I Parent and teacher ratings on the Aberrant Behavior Checklist compared with those of a comparison group*
s
u
Factor
Irritability (Teacher) lrritabiliiy (Parent) Withdrawal (Teacher) Withdrawal (Parent) Overactive (Teacher) Overactive (Parent) Stereotypies (Teacher) Stereotypies (Parent) Inappropriate Speech (Teacher) Inappropriate Speech (Parent)
Patiey (J. T.) Cotnpurison group Prc-op Post-op' Mean (SO)
22
I6 22 0
I
16 30 33 7
37 37 6 0 0 2
6.7 12.0 6.2 4.5 7.1 13.4 2.6 2.2 0.6 2.9
(8.3) (12.0) (9.5) (5.6) (9.9) (10.5) (4.2) (3.7) (1.0) (3.5)
'31 male children aged bciwecn three and 18 years not living in institutions. 'Age 3 years 6 months. 'Age 4 years 6 months.
254
an oligodendroglionia. There was no clinical evidence of seizure recurrence. During the next year, major difficulties included unprovoked aggression and inappropriate behavior, such as attempting to open the family car's door when the car was moving. His parents described him as continuing to be unaware of the affective/ emoiional state of others and showing little observable al'fectivr range himself. However, he began to develop an apparent desire to please his parents and some responsivity to social praise. Although he was reported to know his first and last name, and body parts and to have a vocabulary of at least 100 words, he often talked to himself without particular sentence structure or reasonable contevt. His speech was echolalic and pcrscveraiive. He continued to show abnormalities in peer relationships, with frequent aggressive and/or solitary play. Only rudimentary symbolic play developed. Unusual responses to various sensory stimuli decreased to a moderate extent. Of note wab the development of severe symptoms of hyperactivity, including pervasive motor overactivity, restlessness, inattention, impulsivity, distractability and disruptive behavior. On examination at 4 K years, he was very disiractable, requiring continuous one-to-one focusing to complete the assessment. His head circumference was at [he 95th centile. There were no neurocutaneous stigmata or dysmorphic features. Ncurolo&al examination revealed only mildly increased tone in the ankles, right greater than left. There was no motor weakness. Cerebellar function was age-appropriate. Because an etiology for neurodevelopmenial disability had been established, further diagnostic testing (p.g. cytogenetics) was not done. Echolalia, social avoidance, repetitive behavior and speech with little communicative intent was observed. He was very non-compliant to requests. He had a short attention-span and wds overactive. On several occasions he threw toys and other objects. Using the Stanford-Binet Intelligence Scale LM. subtests from the Wechsler Preschool and Primary Scale of Intelligence-Revised and the Hiskey-
Nebraska Test of Learning Aptitudes (l966), intellectual abilities were found to be in the ranxe of mild to moderate mental retardation. His behavior was assessed with the Aberrant Behavior Checklist (ABC) (Aman and Singh 1986). a scale developed for rating inappropriate and maladaptive behaviors of individuals with developmental disabilities.* The checklist was completed by his parents and special education teacher. In addition, his parent, retrospectively rated his behavior before the tumor resection. Parent and teacher ratings on the ABC were compared with mean scores from a reference group of 31 developmentally disabled male children not living in institutions. using the factor structure reported in Freund and Reiss (1991). These data are presented in Table I . Before the resection, J.T. was rated by his parents as having severe problems, with social withdrawal and isolation at home. I n addition, individual item analysis showed mild or moderate irritability (aggression, temper tantrums, self-injurious behavior) and hyperactivity at home. After tumor resection. difficulties with social withdrawal were noted as being much less prominent at home, but severe at school; hyperactivity was now identified as a severe problem both at home and at school, as was irritabiliiy.
Discussion There is increasing evidence from human and non-human primates that pathological processes affecting the temporal lobe, particularly the amygdala and hippocampus, are related to the development of autistic-like symptomatology. Studies of primates have demonstrated that insults t o regions in the temoral lobe result in 'Items on the ABC are rated from 0 (not a problem) to 3 (severe). Behavioral descriptions fall into five major groupings: irritability, lethargy/social withdrawal, stereotypical behavior, hyperactivity and inappropriate speech.
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TABLE I 1 Diagnostic criteria for DSM-I1I-R autistic disorder in relation to pre- and post-operatiw behatior DSM-Ill-R crilerra
Qualitative impairment in reciprocal tocial interaction ( I ) Marked lack of awareness of the existence or feelings of others (2) No o r abnorinal seeking of comfort at times of d i s t r a t (3) No or impaired inlitation (4) No o r abnormal social play ( 5 ) Gross impairment in ability to make peer friendships B. Qualitative impairment in verbal and non-verbal communication, and in imaginative activity ( I ) N o mode of communicaiioii (2) Markedly abnormal non-verbal communication (3) Absence of imaginative activity (4) Marked abnormalities in the production of speech ( 5 ) Marked abnormalities in the form or content of speech ( 6 ) h,larked impairment in the ability to initiate o r sustain a conversation with others C. Markedly restricted repertoire of activitict and interests ( I ) Stereotyped body movements (2) Persistent preoccupation with parts of objects o r attachment to unusual objects (3) Marked distress over changes in trivial aspects of environment (4) Unreasonable insistcncc on following routines in precise derail ( 5 ) Markedly restricted range o f interests D. Onset during infancy o r childhood
W
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Pre-op'
~osr-op'
Y N Y
N
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A.
'Age 'Age 'Not 'Not
Y NA' N Y Y N A ~ NA"
Y
N Y
NA' N Y N N Y
NA"
NA"
Y
N
Y N N
N Y
N
N N N Y
3 years 6 months. 4 years 6 months. applicable because of developmental le\fel. applicable because of absence of speech.
different sequelae, according to the specific location of the lesion and the developmental period when the insult occurred (Merjanian er a/. 1988, Bachevalier 1991). Our case report provides evidence in humans that unilateral damage to the temporal lobe during early development may lead to the development of a particular subset of autistic features. Before surgery, J.T. met seven of 16 DSM-Ill-R criteria for autism (American Psychiatric Association 1987), including abnormalities in social and affective behavior, communication and response to sensory stimuli (Table 11). Because eight criteria are required for the diagnosis of autistic disorder, the category of pervasive developmental disorder (not otherwise specified) was assigned. However, it should be noted that four of the 16 criteria could not be assessed because of J.T.'S level of developmental skills. After surgery, some of the abnormalities in social and affective behavior persisted, with significant worsening of the hyperactivity and a reduction in unusual responses to sensory stimuli.
Evidence in humans that temporal lobe abnormalities may lead to autistic behavior comes from several sources. There are a number of case reports of autistic behavior associated with temporal lobe damage resulting from herpes encephalitis (DeLong ef al. 1981, Gillberg 1986, Greer et al. 1989). Clinical correlates in herpetic infections have included receptive and expressive language deficits, and disordered behavior with a propensity for physical aggression and memory loss (Greer ef al. 1989). Epidemiological surveys have also noted an association of autism with psychomotor epilepsy (Gillberg 1986). There are several histo-anatomical case reports of microscopic abnormalities in the amygdala and hippocampus on postmortem examination of autistic individuals. Bauman and Kemper reported a 29-year-old male and an 1 1-year-old female whose primary neuro-anatomical abnormalities were confined to the hippocampus, amygdala, entorhinal cortex and cerebellum (Bauman and Kemper 1985, 1987). Engle ef a/. (1989) noted focal gliosis in the left amygdala and hippo-
.
255
Fig. 3. CT scan showing asyttiriierry of subarachnoid spaces (lareral wn!ricles, corrical sulci) a! 6 weeks ojage.
256
campus (right hemisphere not examined), as well as the temporoparietal association cortex, in a 21-year-old female with autism. In primates, damage to the limbic system during infancy leads to behavioral abnormalities analogous to certain behaviors observed in autistic children. The behavioral effects resulting from bilateral ablation of the amygdala and hippocampus in infant monkeys during the first three weeks of life have been described previously (Merjanian er al. 1986, 1988; Bachevalier 1991). At two months of age subtle behavioral changes were noted. Severe social and emotional disturbances, including failure to develop normal social relationships, with isolation and withdrawal, poor eye-contact, abnormal body language, blank facial expression and locomotor stereotypies were not observed until six months of age. In contrast, infant monkeys with anterior, infero-lateral temporal cortical lesions were reported to display prominent hyperactivity and attentional dysfunction at two months of age, which became less severe by six months (Merjanian et a/. 1989).
J . T 's lesion and resection involved similar temporal lobe regions to those of the primate models described above. However, these models typically have involved bilateral temporal lesions, whereas in this case the anatomical lesion was limitcd to the left temporal lobe. Nevertheless, there are several sources of evidence to support the hypothesis that unilateral left temporal lobe lesions in humans may be functionally equivalent to bilateral lesions in primates. I t is known that the amygdala has numerous connections through the anterior commissure with the corresponding contralateral region (Brodal 1981); therefore dysfunction on one side may be reflected in the contralateral structure. Evidence for bilateral temporal lobe effects from a unilateral lesion or resection has also been described in humans with temporal lobe tumors. Cavazzuti et al. (1980) reported that nine patients with tumors resected from the left (dominant) temporal lobe had postoperative improvements in short-term and delayed non-verbal memory processes, functions which are usually ascribed to the non-dominant lobe. These changes were in additon to the increased verbal (dominant lobe) dysfunction seen after resection. None of these patients had clinical or radiographic evidence of elevated intracranial pressure which might have accounted for the change in contralateral temporal lobe function. Finally, the human brain is distinguished from that of non-human primates largely by the marked hemispheric asymmetry which underlies specialized functions such as language (Mesulam 1985). This increases the likelihood of more significant effects resulting from unilateral damage to structures involved in hemispheric dominance patterns in humans. This may be especially true when these structures are affected during specific, early developmental stages. For the child described in this report, persistent developmental problems included abnormalities of recognition and demonstration of affect, as well as verbal and non-verbal communication deficits. These clinical features are consistent with the proposed involvement of the amygdala and hippocampus in the
regulation and integration of affect, memory and learning (Mesulam 1985). Oligodendrogliomata such as the one in this case comprise only 5 per cent of all primary brain tumors and are uncommon during infancy (Mork el al. 1985, Tomita a n d M c L o n e 1985). The size of J.T.’S lesion was estimated to be 31cm3 on Tpweighted coronal and axial images, using a Macintosh 11-based Image Analysis Workstation. Although the biological behavior of any neoplasm is usually unknown, the early increased head size and onset of neurobehavioral abnormalities, as well as the large size of the tumor, suggest that it may have been present very early in life (Tomita and McLone 1985). When reviewed retrospectively, the CT scan at six weeks of age showed asymmetry of the subarachnoid spaces, including the lateral ventricle, Sylvian fissure and cortical sulci (Fig. 3). Recognizing the limitations of retrospective data collection in this case, we assume that early damage to left mesialtemporal structures, particularly the amygdala and hippocampus, disrupted functional neuro-anatomical pathways involved in the development of normal affective and social behavior, verbal and non-verbal communication, and modulation of response to sensory stimuli. The neurobehavioral abnormalities which developed are consistent with the diagnosis of pervasive developmental disorder. Although the seizure disorder, first noted at two years of age, may have affected J.T.’S developmental course, these seizures d o not account for the neurobehavioral
abnormalities that were present before that age, or for the qualitative abnormalities of development that persisted after the resection. The portion of the inferolateral left temporal lobe removed during resection c o r r e s p o n d s to the region that, when damaged early in development, gives rise to a transient hyperactivity syndrome in primates (Merjanian et al. 1989). It is possible that the removal of this region may have contributed to the significant increase in hyperactivity observed in J.T. after surgery. In summary, this case contributes additional evidence to the hypothesis that early damage to mesial-temporal structures increases the risk for development of social, communicative and sensory components of the autistic behavioral syndrome.
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Accepred f o r publicarron 3rd Ocrober 1991. Acknowledgemenis This work was supported by grant MH00726 from the National Institute of Mental Health, grant HD24061, a Biomedical Research Grant from the National Institute of Health, and a grant from the John Merck Fund (Dr. Reiss). The authors thank Drs. Jocelyne Bachevalier. Arnold Capute. Benjamin Car5on. Martha Denckla, Lynne Huffman and Ms. Carol James for their help during the preparation of this manuscript. Auihors’ Appoiniments *Alexander H. Hoon, Jr., M.D., Department of Developmental Pediatrics, The Kennedy Institute, 707 North Broadway, Baltimore, MD 21205. Allan L. Reiss, M.D., Neuroirnaging Center, The Kennedy Institute; Division of Child Psychiatry and Department of Psychiatry, The Johns Hopkins University School of Medicine. *Correspondence lo frrsi author.
SUMMARY Human and non-human primate research has shown that pathological processes affecting the temporal lobe, particularly the amygdala and hippocampus, are related to the development of the autistic syndrome. This case report describes a young male child with left temporal oligodendroglioma, who demonstrated a constellation of autistic behaviors meeting DSM-Ill-R criteria for pervasive developmental disorder. Abnormalities in social interaction, affective expression and communication were particularly evident. Some of the symptoms improved after tumor resection, while other signs of qualitative abnormalities in development emerged or persisted. This case adds evidence to the hypothesis that damage to mesial-temporal structures at an early developmental period may lead to the autistic syndrome. RESUME Lobe ieniporal median er auiisme: rapport d’itri cas el revue de la lirierature Les recherches chez le primate humain et non-humain ont montre que les processus pathologiques affectant le lobe temporal, particulierement I’amygdale et I’hippocampe, sont lies au developpement du syndrome autistique. L’article decrit un jeune garcon presentant un oligodendrogliome exprimant divers comportements autistiques repondant aux criteres du DSM-Ill-R pour le trouble invasif du developpement. Des anomalies dans les interactions sociales, I’expression affective et la communication itient particulierement evidentes. Certains de ces symtbmes regresserent apres la
25 7
resection de la tumcur alors que d’autres signcs d’anomalies qualitatives du devcloppement apparaissaicnt ou persistaient. Cc cas apporte un argument supplemcntaire a I’hypothese qui voit dans les lesions des structures mCdio-temporales a un stade prCcoce du developpemcnt, unc cause de syndrome autistiquc. ZUSAMMENFASSUNG Der tnesiule A nreil des Tetnporullappen.~l i t i d Aurisriiits: Fallbesdireibutig iold Uberlilick Forschungen an Menschen und Primaten haben gezeigt, dan pathologische Prozesse, dic den Temporallappen, insbcsondere Amygdala und Hippocapmus betreffcn, niit der Entivicklung dcs autistischen Syndronis vcrbunden sind. Dieser Fallbericht bcschrcibt einen Jungen mit cincm Oligodendrogliom links tcmporal, bei dem ein autistichcs Vcrhalten auffiel, das dic DSM-Ill-R Kritcricn fur pervasive Entwicklungsstorungen erfulltc. Anomalien bei sozialen Intcraktionen, Gefulsauflerungcn und Kommunikationen waren besonderh auffdllig. Einige dieser Symptomc besscrtcn sich nach Resektion dcs Tumors, wahrend andcrc abnorme Refunde in dcr Ent\vicklung auftratcn odcr persistierten. Dicscr Fall s t u t ~ die t Hypothesc, dafl cine Schddigung von Strukturen dcs mcsialen Temporallappens in dcr fruhen Entwicklungsphasc zu einem autistischcn Syndrom fuhren kann.
R ESU M EN Parre medial del lobulo temporal y aitristno: uporlacion de i r n caso .v revision Invcstigaciones realizadas en humanos y primates han mostrado que procesos patologicos afectando el lobulo temporal, especialmcntc la amigdala y el hipocanipo, cstan en relacion con cl dcsarrollo de un sindrome autistico. El caso aportado es el de un muchacho con un oligodcndroglioma temporal izquicrdo, que exhibia una constclacion d e comportamicntos autisticos dc acuerdo con 10s critcrios dc DSM-Ill-R para las altcracioncs pervasivas del desarrollo. Eran especialmentc cvidentes la anomalias en la intcraccion social y en la expression y communicacion afectiva. Alguno dc estos sintonias mcjoraron despues dc la cxtirpacion del tumor, micntras que aparccicron o persiitieron otrot signos d e anomalias dcl dcsarrollo. Este caso afiadc cvidencia a la hipotcsis dc que la lesion dc las cstruciuras mediales dcl lobulo temporal, en una fase precoz del desarrollo, pueden conducir a un sindrome autistico.
258
References Anian, M. G., Singh, N. N. (1986) Aberranr Behavior Cliecklisr Munual. East Aurora, NY: Slosson Educational Publication\. American Psychiatric Association (1987) Diugnosric and Sla/isrical Manirul of Mcnral Disorders. Third Edn., Revised. Washington, DC: A.P.A. Bachevalier. J . (1991) ‘An animal model for childhood autism: mcmory loss and socioemotional disturbanccs following neonatal damage to the limbic syttcm in monkeys.’ In Tamminga, C. A., Schultz, S. C. (Eds.) Advances in Neurops.vchiarry and Psyclropliurtiiaco1og.v Schizophrenia Research. New York: Raven Press. Bauman, M.. Kcmper, T. L. (1985) ‘Histoanatomic observations of thc brain in early infantile autism.’ Neurology, 35, 866-874. - - (1987) ‘Limbic involvement in a second case of early infantile autism.’ Neurology, 37 (Suppl. I), 147. Brodal, A. (1981) ‘The olfactory parhways, thc amygdala, the hippocampus, the “limbic system”.’ In Neurological Anaioniy in Relarion 10 Clinical Medicine, Third Edn. New York: Oxford Universiry Press. Cavazzuti, V . , Winston, K., Baker. R., Welch, K . (1980) ‘Psychological changes following surgery for tumors in the temporal lobe.’ Journal of Neurosurgery. 53, 6 18-626. Chess. S. (1971) ‘Autism in children w,irh congenital rubclla.’ Journul of Aurisni and Childhood Schizophrenia, I , 33-44. Courchesne, E., Yeung-Courchesnc, R., Press, G. A,, Hessclink, J . R.,. Jernizan, T. L. (1988) ‘Hypoplasia of cyebellai vermal lobules VI and VII in autism. New England Journal of Medicine, 31 8, 1349- 1354. Damasio, A. R., Maurcr, R. G. (1978) ‘A neurological model for childhood autism.’ Archives of Neurology. 35, 7 71-786. DcLong. G. R., Bean, S. C.. Brown, F. R . (1981)
‘Acquired reversible autistic syndrome in acute cncephalopathic illncss in children.’ Archives of Neurology, 38, 191-194. Engle, E. C.. Kowall, N. W., McKee, A . C. (1989) ‘Focal gliosis in the amygdala and temperoparietal association cortex in a rctarded woman with autism.’ Society f o r Neuroscience AbsrracrJ. 15(2), 1334. Freund, L., Reiss, A. L. (1991) ‘Rating problem behaviour in outpatients with mental retardation: use of the Aberrant Behavior Checklist.’ Research in Developnienral Disabiliries, 12, 435-45 1 . Gillberg, C. (1986) ‘Brief report: onset at age 14 of a typical autistic syndrome. A case report of a girl with hcrpcs simplex enccphalitis.’ Journal of A uristn and Develop~nenrul Disorders, 16, 369-375. Greer, M. K., Lyons-Crews, M., Mauldin, L. B.. Brown, F. R . (1989) ‘A ca$e study of the cognitive and behavioral deficits of temporal lobe damage in hcrpes simplex encephalitis.’ Journal of Aulisin nnd Dcvclopmenrul Disorders, 19, 317-326. Hiskey-Nebraska Tes! of Learning Aptitudes (1966) Lincoln Nebraska: Union College Press. Merjanian, P. M., Bachevalicr, J., Crawford, H., Mishkin, M. (1986) ‘Socio-emotional disturbances in the developing rhesus monkey following neonatal limbic lesions.’ Sociery f o r Neuroscience Absrracrs, 12(1), 23. - - Pettigrew, D., Mishkin, M. (1988) ‘Developmental time course, as well as nature of socio-emotional disturbances in rhesus monkeys following neonatal limbic lesions resemble those in autism.’ Sociery for Neuroscience Absrracrs. 14(1), 2. - - _ (1989) ‘Behavioral disturbances in the developing rhesus monkey following neonatal lesions of interior temporal cortex (area TE) resemble those in attention-deficit hyperactivity
disorder.’ Sociery j o r Neuroscience Abstracts, 15(1), 302. blesulam, hl.-M. (1985) ‘Patterns in behavioral neuroanatomy: association areas, the limbic system and hemispheric specialisat ion. In Principles of Behavioral Neurology. Philadelphia: F. A. Davis. Mork. S. J.. Lindcgaard, K . , Halvorsen, T. B., Lehmann, E. H., Solgaard, T., Hatlevoll, R., Harvci, S., Ganz, J . (1985) ‘Oligodendroglioma: incidence and biological bchavior in ,a defined
. population.’ Journal of Neurosurgery, 63,
Visual Hallucinations after Acute Visual Loss in a Young Child
glioma) an 18-month course of chemotherapy was instituted. At the age of 2 % years his.optic discs were noted to be pale and his recognition visual acuity was 6/30 in both eyes. There were no other neurological abnormalities and he was otherwise well. CT scanning showed the tumour to have not increased in size. At the age of 3’1: years he was found to have a left temporal ficld loss, with no change in visual acuity. Over the next six months his vision gradually deteriorated until he had only light perception in his right eye and 6/60 in his left eye with severe peripheral field loss. A repeat C T scan revealed an increase in rhe size of the tumour and it was decided to recommence chemotherapy and debulk thc tumour. After surgery the child was torally blind; the postopcrative course otherwise was uneventful. One week after the operation he suddenly began to experience visual hallucinations: he saw people, including his brother and Santa Claus, animals and other familiar objects. The hallucinations moved around in both visual fields. They lasted for three days, abating only in sleep. No provoking factors were identified. There were no auditory, olfactory or tactile accompaniments. Initially he was frightened by the hallucinations, and became angry when told that they were imaginary. There was no previous history of visual hallucinations. The child’s mental status appeared normal apart from the visual hallucinations, and neurological and fundoscopic examinations were unchanged apart from the sudden visual loss. He was receiving no. medication and was afebrile. There was no evidence of ‘electrolyte imbalance o r other pituitary dysfunction. An electroencephalogram was normal and a repeat C T scan showed a significant reduction in the size of the tumour, but no new abnormalities.
C. P. White J. E. Jan
’
Visual hallucinations are common manifestations of toxic confusional states and psychoses. They may also arise secondary to lesions of the visual pathway anywhere from the eye to the cortex in otherwise healthy people. They are most commonly reported in older individuals with gradually deteriorating vision from a variety of causes, and are thought of as release phenomena (Cogan 1973). Rarely, they may be a manifestation of seizure activity in the occipital or temporal regions (Russell and Whitty 1955, Lance 1976). Hallucinations with visual loss have not been reported previously in young children.
Case report At the age of I 1 months the patient presented with a four-week history of nysragmus. Pregnancy and delivery had been normal, as had been his development until that time. Initial cxamination revealed the presence of an involuntary, bilateral, conjugate nystagmus of similar amplitude in both eyes. The horizontal nature of the nystagmus was maintained in upgaze. Neurological examination was unremarkable and there was no evidence of neurofibromatosis. A C T scan revealed the presence of a large suprasellar tumour extending posteriorly along the optic radiations. Following stereotactic biopsy (confirming the presence o f a low-grade optic
881-889. Ornitz, E. M. (1985) ‘Neurophysiology of infantile autism.’ Journal o/ rhe Amerjcan Acadenty of Child Psychiatry, 24, 25 1-262. Reiss. A. L., Fcinstein, C., Rosenbaum, K . N. (1986) ‘Autism and genetic disorders.’ Schizophrenia Bulletin, 12, 724-738. Tomira, T.. McLone, D. G . (1985) ‘Brain tumors during the first twenty-four months of life.’ Neurosurgery, 17, 913-919.
Discussion In 1769 Charles Bonnet published an account of the visual hallucinations experienced by his grandfather, an 89year-old man with severely decreased visual ‘acuity as a result of bilateral cataracts, who otherwise was in excellent physical and mental health. Since then there have been a number of other reports of such phenomena occurring in individuals, especially the elderly, in the absence of psychiatric disorder (DamasMora el al. 1982, Olbrich et al. 1987), and
m v.
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259
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Autism is the prototypal disorder in the class of neuropsychiatric diseases known as pervasive developmental disorders. The behavioral syndrome of autism consists of significant abnormalities in social interaction, behavior and communication. Mental retardation is usual, but not invariable. Despite research on human and animal models, little is known of the specific neurobiological factors directly responsible for the pathogenesis of autism. Autism has been associated with a number of medical conditions, including congenital rubella, herpes encephalitis, fragile-x syndrome, tuberous sclerosis, neurofibromatosis and phenylketonuria (Chess 1971, Reiss ef al. 1986). Neuropathological and brain-imaging abnormalities in cases with and without presumed biological etiology have led to neurophysiological hypotheses linking dysfunction of various areas of the brain t o autism. These areas include the temporal lobe (Damasio and Maurer 1978), cerebellum (Courchesne ef al. 1988) and brainstem (Ornitz 1985).
In this case report we describe a young male child with a left temporal oligodendroglioma, who demonstrated a constellation of autistic behaviors meeting DSMI l l - R criteria for pervasive developmental 252
disorder. Some of these a u t i s t i c symptoms
resolved after resection, while other qualitative signs of developmental abnormality emerged or persisted. Given reports of human neuropathology and animal models indicating an association between temporal lobe lesions and autism, we believe that the tumor disrupted normal neurodevelopment, resulting in a clinical picture which included autistic behavior. Clinical and neuro-anatomical features of this case are presented to add to the understanding of the neurobiological basis of autistic behavior.
Case report J.T. was born to a 32-year-old gravida 2 woman. Pregnancy was complicated by symptomatically managed ulcerative colitis, for which she look prednisone during the first six weeks of pregnancy. Fetal activity was described as normal in onset and quality. There were no infections or exposure to teratogens. Weight gain was I I .35kg. He was delivered at 39 weeks gestation, with birthweight and head circumference at the 60th and 75th centiles, respectively. Although there were mild signs of fetal distress at delivery, no resuscitation was required. He was discharged h o m c on t h e second post-partum day. A head CT scan was performed at six weeks of age because of rapid increase in head circumference to the 95th centile. The results were interpreted as normal at that time, although retrospective evaluation of this scan suggested abnormalities (discussed below). There was no subsequent abnormal increase in head size.
s-52
n 4
TABLE I Parent and teacher ratings on the Aberrant Behavior Checklist compared with those of a comparison group*
s
u
Factor
Irritability (Teacher) lrritabiliiy (Parent) Withdrawal (Teacher) Withdrawal (Parent) Overactive (Teacher) Overactive (Parent) Stereotypies (Teacher) Stereotypies (Parent) Inappropriate Speech (Teacher) Inappropriate Speech (Parent)
Patiey (J. T.) Cotnpurison group Prc-op Post-op' Mean (SO)
22
I6 22 0
I
16 30 33 7
37 37 6 0 0 2
6.7 12.0 6.2 4.5 7.1 13.4 2.6 2.2 0.6 2.9
(8.3) (12.0) (9.5) (5.6) (9.9) (10.5) (4.2) (3.7) (1.0) (3.5)
'31 male children aged bciwecn three and 18 years not living in institutions. 'Age 3 years 6 months. 'Age 4 years 6 months.
254
an oligodendroglionia. There was no clinical evidence of seizure recurrence. During the next year, major difficulties included unprovoked aggression and inappropriate behavior, such as attempting to open the family car's door when the car was moving. His parents described him as continuing to be unaware of the affective/ emoiional state of others and showing little observable al'fectivr range himself. However, he began to develop an apparent desire to please his parents and some responsivity to social praise. Although he was reported to know his first and last name, and body parts and to have a vocabulary of at least 100 words, he often talked to himself without particular sentence structure or reasonable contevt. His speech was echolalic and pcrscveraiive. He continued to show abnormalities in peer relationships, with frequent aggressive and/or solitary play. Only rudimentary symbolic play developed. Unusual responses to various sensory stimuli decreased to a moderate extent. Of note wab the development of severe symptoms of hyperactivity, including pervasive motor overactivity, restlessness, inattention, impulsivity, distractability and disruptive behavior. On examination at 4 K years, he was very disiractable, requiring continuous one-to-one focusing to complete the assessment. His head circumference was at [he 95th centile. There were no neurocutaneous stigmata or dysmorphic features. Ncurolo&al examination revealed only mildly increased tone in the ankles, right greater than left. There was no motor weakness. Cerebellar function was age-appropriate. Because an etiology for neurodevelopmenial disability had been established, further diagnostic testing (p.g. cytogenetics) was not done. Echolalia, social avoidance, repetitive behavior and speech with little communicative intent was observed. He was very non-compliant to requests. He had a short attention-span and wds overactive. On several occasions he threw toys and other objects. Using the Stanford-Binet Intelligence Scale LM. subtests from the Wechsler Preschool and Primary Scale of Intelligence-Revised and the Hiskey-
Nebraska Test of Learning Aptitudes (l966), intellectual abilities were found to be in the ranxe of mild to moderate mental retardation. His behavior was assessed with the Aberrant Behavior Checklist (ABC) (Aman and Singh 1986). a scale developed for rating inappropriate and maladaptive behaviors of individuals with developmental disabilities.* The checklist was completed by his parents and special education teacher. In addition, his parent, retrospectively rated his behavior before the tumor resection. Parent and teacher ratings on the ABC were compared with mean scores from a reference group of 31 developmentally disabled male children not living in institutions. using the factor structure reported in Freund and Reiss (1991). These data are presented in Table I . Before the resection, J.T. was rated by his parents as having severe problems, with social withdrawal and isolation at home. I n addition, individual item analysis showed mild or moderate irritability (aggression, temper tantrums, self-injurious behavior) and hyperactivity at home. After tumor resection. difficulties with social withdrawal were noted as being much less prominent at home, but severe at school; hyperactivity was now identified as a severe problem both at home and at school, as was irritabiliiy.
Discussion There is increasing evidence from human and non-human primates that pathological processes affecting the temporal lobe, particularly the amygdala and hippocampus, are related to the development of autistic-like symptomatology. Studies of primates have demonstrated that insults t o regions in the temoral lobe result in 'Items on the ABC are rated from 0 (not a problem) to 3 (severe). Behavioral descriptions fall into five major groupings: irritability, lethargy/social withdrawal, stereotypical behavior, hyperactivity and inappropriate speech.
v)
TABLE I 1 Diagnostic criteria for DSM-I1I-R autistic disorder in relation to pre- and post-operatiw behatior DSM-Ill-R crilerra
Qualitative impairment in reciprocal tocial interaction ( I ) Marked lack of awareness of the existence or feelings of others (2) No o r abnorinal seeking of comfort at times of d i s t r a t (3) No or impaired inlitation (4) No o r abnormal social play ( 5 ) Gross impairment in ability to make peer friendships B. Qualitative impairment in verbal and non-verbal communication, and in imaginative activity ( I ) N o mode of communicaiioii (2) Markedly abnormal non-verbal communication (3) Absence of imaginative activity (4) Marked abnormalities in the production of speech ( 5 ) Marked abnormalities in the form or content of speech ( 6 ) h,larked impairment in the ability to initiate o r sustain a conversation with others C. Markedly restricted repertoire of activitict and interests ( I ) Stereotyped body movements (2) Persistent preoccupation with parts of objects o r attachment to unusual objects (3) Marked distress over changes in trivial aspects of environment (4) Unreasonable insistcncc on following routines in precise derail ( 5 ) Markedly restricted range o f interests D. Onset during infancy o r childhood
W
N I N N v)
Pre-op'
~osr-op'
Y N Y
N
%
A.
'Age 'Age 'Not 'Not
Y NA' N Y Y N A ~ NA"
Y
N Y
NA' N Y N N Y
NA"
NA"
Y
N
Y N N
N Y
N
N N N Y
3 years 6 months. 4 years 6 months. applicable because of developmental le\fel. applicable because of absence of speech.
different sequelae, according to the specific location of the lesion and the developmental period when the insult occurred (Merjanian er a/. 1988, Bachevalier 1991). Our case report provides evidence in humans that unilateral damage to the temporal lobe during early development may lead to the development of a particular subset of autistic features. Before surgery, J.T. met seven of 16 DSM-Ill-R criteria for autism (American Psychiatric Association 1987), including abnormalities in social and affective behavior, communication and response to sensory stimuli (Table 11). Because eight criteria are required for the diagnosis of autistic disorder, the category of pervasive developmental disorder (not otherwise specified) was assigned. However, it should be noted that four of the 16 criteria could not be assessed because of J.T.'S level of developmental skills. After surgery, some of the abnormalities in social and affective behavior persisted, with significant worsening of the hyperactivity and a reduction in unusual responses to sensory stimuli.
Evidence in humans that temporal lobe abnormalities may lead to autistic behavior comes from several sources. There are a number of case reports of autistic behavior associated with temporal lobe damage resulting from herpes encephalitis (DeLong ef al. 1981, Gillberg 1986, Greer et al. 1989). Clinical correlates in herpetic infections have included receptive and expressive language deficits, and disordered behavior with a propensity for physical aggression and memory loss (Greer ef al. 1989). Epidemiological surveys have also noted an association of autism with psychomotor epilepsy (Gillberg 1986). There are several histo-anatomical case reports of microscopic abnormalities in the amygdala and hippocampus on postmortem examination of autistic individuals. Bauman and Kemper reported a 29-year-old male and an 1 1-year-old female whose primary neuro-anatomical abnormalities were confined to the hippocampus, amygdala, entorhinal cortex and cerebellum (Bauman and Kemper 1985, 1987). Engle ef a/. (1989) noted focal gliosis in the left amygdala and hippo-
.
255
Fig. 3. CT scan showing asyttiriierry of subarachnoid spaces (lareral wn!ricles, corrical sulci) a! 6 weeks ojage.
256
campus (right hemisphere not examined), as well as the temporoparietal association cortex, in a 21-year-old female with autism. In primates, damage to the limbic system during infancy leads to behavioral abnormalities analogous to certain behaviors observed in autistic children. The behavioral effects resulting from bilateral ablation of the amygdala and hippocampus in infant monkeys during the first three weeks of life have been described previously (Merjanian er al. 1986, 1988; Bachevalier 1991). At two months of age subtle behavioral changes were noted. Severe social and emotional disturbances, including failure to develop normal social relationships, with isolation and withdrawal, poor eye-contact, abnormal body language, blank facial expression and locomotor stereotypies were not observed until six months of age. In contrast, infant monkeys with anterior, infero-lateral temporal cortical lesions were reported to display prominent hyperactivity and attentional dysfunction at two months of age, which became less severe by six months (Merjanian et a/. 1989).
J . T 's lesion and resection involved similar temporal lobe regions to those of the primate models described above. However, these models typically have involved bilateral temporal lesions, whereas in this case the anatomical lesion was limitcd to the left temporal lobe. Nevertheless, there are several sources of evidence to support the hypothesis that unilateral left temporal lobe lesions in humans may be functionally equivalent to bilateral lesions in primates. I t is known that the amygdala has numerous connections through the anterior commissure with the corresponding contralateral region (Brodal 1981); therefore dysfunction on one side may be reflected in the contralateral structure. Evidence for bilateral temporal lobe effects from a unilateral lesion or resection has also been described in humans with temporal lobe tumors. Cavazzuti et al. (1980) reported that nine patients with tumors resected from the left (dominant) temporal lobe had postoperative improvements in short-term and delayed non-verbal memory processes, functions which are usually ascribed to the non-dominant lobe. These changes were in additon to the increased verbal (dominant lobe) dysfunction seen after resection. None of these patients had clinical or radiographic evidence of elevated intracranial pressure which might have accounted for the change in contralateral temporal lobe function. Finally, the human brain is distinguished from that of non-human primates largely by the marked hemispheric asymmetry which underlies specialized functions such as language (Mesulam 1985). This increases the likelihood of more significant effects resulting from unilateral damage to structures involved in hemispheric dominance patterns in humans. This may be especially true when these structures are affected during specific, early developmental stages. For the child described in this report, persistent developmental problems included abnormalities of recognition and demonstration of affect, as well as verbal and non-verbal communication deficits. These clinical features are consistent with the proposed involvement of the amygdala and hippocampus in the
regulation and integration of affect, memory and learning (Mesulam 1985). Oligodendrogliomata such as the one in this case comprise only 5 per cent of all primary brain tumors and are uncommon during infancy (Mork el al. 1985, Tomita a n d M c L o n e 1985). The size of J.T.’S lesion was estimated to be 31cm3 on Tpweighted coronal and axial images, using a Macintosh 11-based Image Analysis Workstation. Although the biological behavior of any neoplasm is usually unknown, the early increased head size and onset of neurobehavioral abnormalities, as well as the large size of the tumor, suggest that it may have been present very early in life (Tomita and McLone 1985). When reviewed retrospectively, the CT scan at six weeks of age showed asymmetry of the subarachnoid spaces, including the lateral ventricle, Sylvian fissure and cortical sulci (Fig. 3). Recognizing the limitations of retrospective data collection in this case, we assume that early damage to left mesialtemporal structures, particularly the amygdala and hippocampus, disrupted functional neuro-anatomical pathways involved in the development of normal affective and social behavior, verbal and non-verbal communication, and modulation of response to sensory stimuli. The neurobehavioral abnormalities which developed are consistent with the diagnosis of pervasive developmental disorder. Although the seizure disorder, first noted at two years of age, may have affected J.T.’S developmental course, these seizures d o not account for the neurobehavioral
abnormalities that were present before that age, or for the qualitative abnormalities of development that persisted after the resection. The portion of the inferolateral left temporal lobe removed during resection c o r r e s p o n d s to the region that, when damaged early in development, gives rise to a transient hyperactivity syndrome in primates (Merjanian et al. 1989). It is possible that the removal of this region may have contributed to the significant increase in hyperactivity observed in J.T. after surgery. In summary, this case contributes additional evidence to the hypothesis that early damage to mesial-temporal structures increases the risk for development of social, communicative and sensory components of the autistic behavioral syndrome.
‘c)
N \o N ‘c)
N
2 No\
Q‘
3
2
0
3-
Accepred f o r publicarron 3rd Ocrober 1991. Acknowledgemenis This work was supported by grant MH00726 from the National Institute of Mental Health, grant HD24061, a Biomedical Research Grant from the National Institute of Health, and a grant from the John Merck Fund (Dr. Reiss). The authors thank Drs. Jocelyne Bachevalier. Arnold Capute. Benjamin Car5on. Martha Denckla, Lynne Huffman and Ms. Carol James for their help during the preparation of this manuscript. Auihors’ Appoiniments *Alexander H. Hoon, Jr., M.D., Department of Developmental Pediatrics, The Kennedy Institute, 707 North Broadway, Baltimore, MD 21205. Allan L. Reiss, M.D., Neuroirnaging Center, The Kennedy Institute; Division of Child Psychiatry and Department of Psychiatry, The Johns Hopkins University School of Medicine. *Correspondence lo frrsi author.
SUMMARY Human and non-human primate research has shown that pathological processes affecting the temporal lobe, particularly the amygdala and hippocampus, are related to the development of the autistic syndrome. This case report describes a young male child with left temporal oligodendroglioma, who demonstrated a constellation of autistic behaviors meeting DSM-Ill-R criteria for pervasive developmental disorder. Abnormalities in social interaction, affective expression and communication were particularly evident. Some of the symptoms improved after tumor resection, while other signs of qualitative abnormalities in development emerged or persisted. This case adds evidence to the hypothesis that damage to mesial-temporal structures at an early developmental period may lead to the autistic syndrome. RESUME Lobe ieniporal median er auiisme: rapport d’itri cas el revue de la lirierature Les recherches chez le primate humain et non-humain ont montre que les processus pathologiques affectant le lobe temporal, particulierement I’amygdale et I’hippocampe, sont lies au developpement du syndrome autistique. L’article decrit un jeune garcon presentant un oligodendrogliome exprimant divers comportements autistiques repondant aux criteres du DSM-Ill-R pour le trouble invasif du developpement. Des anomalies dans les interactions sociales, I’expression affective et la communication itient particulierement evidentes. Certains de ces symtbmes regresserent apres la
25 7
resection de la tumcur alors que d’autres signcs d’anomalies qualitatives du devcloppement apparaissaicnt ou persistaient. Cc cas apporte un argument supplemcntaire a I’hypothese qui voit dans les lesions des structures mCdio-temporales a un stade prCcoce du developpemcnt, unc cause de syndrome autistiquc. ZUSAMMENFASSUNG Der tnesiule A nreil des Tetnporullappen.~l i t i d Aurisriiits: Fallbesdireibutig iold Uberlilick Forschungen an Menschen und Primaten haben gezeigt, dan pathologische Prozesse, dic den Temporallappen, insbcsondere Amygdala und Hippocapmus betreffcn, niit der Entivicklung dcs autistischen Syndronis vcrbunden sind. Dieser Fallbericht bcschrcibt einen Jungen mit cincm Oligodendrogliom links tcmporal, bei dem ein autistichcs Vcrhalten auffiel, das dic DSM-Ill-R Kritcricn fur pervasive Entwicklungsstorungen erfulltc. Anomalien bei sozialen Intcraktionen, Gefulsauflerungcn und Kommunikationen waren besonderh auffdllig. Einige dieser Symptomc besscrtcn sich nach Resektion dcs Tumors, wahrend andcrc abnorme Refunde in dcr Ent\vicklung auftratcn odcr persistierten. Dicscr Fall s t u t ~ die t Hypothesc, dafl cine Schddigung von Strukturen dcs mcsialen Temporallappens in dcr fruhen Entwicklungsphasc zu einem autistischcn Syndrom fuhren kann.
R ESU M EN Parre medial del lobulo temporal y aitristno: uporlacion de i r n caso .v revision Invcstigaciones realizadas en humanos y primates han mostrado que procesos patologicos afectando el lobulo temporal, especialmcntc la amigdala y el hipocanipo, cstan en relacion con cl dcsarrollo de un sindrome autistico. El caso aportado es el de un muchacho con un oligodcndroglioma temporal izquicrdo, que exhibia una constclacion d e comportamicntos autisticos dc acuerdo con 10s critcrios dc DSM-Ill-R para las altcracioncs pervasivas del desarrollo. Eran especialmentc cvidentes la anomalias en la intcraccion social y en la expression y communicacion afectiva. Alguno dc estos sintonias mcjoraron despues dc la cxtirpacion del tumor, micntras que aparccicron o persiitieron otrot signos d e anomalias dcl dcsarrollo. Este caso afiadc cvidencia a la hipotcsis dc que la lesion dc las cstruciuras mediales dcl lobulo temporal, en una fase precoz del desarrollo, pueden conducir a un sindrome autistico.
258
References Anian, M. G., Singh, N. N. (1986) Aberranr Behavior Cliecklisr Munual. East Aurora, NY: Slosson Educational Publication\. American Psychiatric Association (1987) Diugnosric and Sla/isrical Manirul of Mcnral Disorders. Third Edn., Revised. Washington, DC: A.P.A. Bachevalier. J . (1991) ‘An animal model for childhood autism: mcmory loss and socioemotional disturbanccs following neonatal damage to the limbic syttcm in monkeys.’ In Tamminga, C. A., Schultz, S. C. (Eds.) Advances in Neurops.vchiarry and Psyclropliurtiiaco1og.v Schizophrenia Research. New York: Raven Press. Bauman, M.. Kcmper, T. L. (1985) ‘Histoanatomic observations of thc brain in early infantile autism.’ Neurology, 35, 866-874. - - (1987) ‘Limbic involvement in a second case of early infantile autism.’ Neurology, 37 (Suppl. I), 147. Brodal, A. (1981) ‘The olfactory parhways, thc amygdala, the hippocampus, the “limbic system”.’ In Neurological Anaioniy in Relarion 10 Clinical Medicine, Third Edn. New York: Oxford Universiry Press. Cavazzuti, V . , Winston, K., Baker. R., Welch, K . (1980) ‘Psychological changes following surgery for tumors in the temporal lobe.’ Journal of Neurosurgery. 53, 6 18-626. Chess. S. (1971) ‘Autism in children w,irh congenital rubclla.’ Journul of Aurisni and Childhood Schizophrenia, I , 33-44. Courchesne, E., Yeung-Courchesnc, R., Press, G. A,, Hessclink, J . R.,. Jernizan, T. L. (1988) ‘Hypoplasia of cyebellai vermal lobules VI and VII in autism. New England Journal of Medicine, 31 8, 1349- 1354. Damasio, A. R., Maurcr, R. G. (1978) ‘A neurological model for childhood autism.’ Archives of Neurology. 35, 7 71-786. DcLong. G. R., Bean, S. C.. Brown, F. R . (1981)
‘Acquired reversible autistic syndrome in acute cncephalopathic illncss in children.’ Archives of Neurology, 38, 191-194. Engle, E. C.. Kowall, N. W., McKee, A . C. (1989) ‘Focal gliosis in the amygdala and temperoparietal association cortex in a rctarded woman with autism.’ Society f o r Neuroscience AbsrracrJ. 15(2), 1334. Freund, L., Reiss, A. L. (1991) ‘Rating problem behaviour in outpatients with mental retardation: use of the Aberrant Behavior Checklist.’ Research in Developnienral Disabiliries, 12, 435-45 1 . Gillberg, C. (1986) ‘Brief report: onset at age 14 of a typical autistic syndrome. A case report of a girl with hcrpcs simplex enccphalitis.’ Journal of A uristn and Develop~nenrul Disorders, 16, 369-375. Greer, M. K., Lyons-Crews, M., Mauldin, L. B.. Brown, F. R . (1989) ‘A ca$e study of the cognitive and behavioral deficits of temporal lobe damage in hcrpes simplex encephalitis.’ Journal of Aulisin nnd Dcvclopmenrul Disorders, 19, 317-326. Hiskey-Nebraska Tes! of Learning Aptitudes (1966) Lincoln Nebraska: Union College Press. Merjanian, P. M., Bachevalicr, J., Crawford, H., Mishkin, M. (1986) ‘Socio-emotional disturbances in the developing rhesus monkey following neonatal limbic lesions.’ Sociery f o r Neuroscience Absrracrs, 12(1), 23. - - Pettigrew, D., Mishkin, M. (1988) ‘Developmental time course, as well as nature of socio-emotional disturbances in rhesus monkeys following neonatal limbic lesions resemble those in autism.’ Sociery for Neuroscience Absrracrs. 14(1), 2. - - _ (1989) ‘Behavioral disturbances in the developing rhesus monkey following neonatal lesions of interior temporal cortex (area TE) resemble those in attention-deficit hyperactivity
disorder.’ Sociery j o r Neuroscience Abstracts, 15(1), 302. blesulam, hl.-M. (1985) ‘Patterns in behavioral neuroanatomy: association areas, the limbic system and hemispheric specialisat ion. In Principles of Behavioral Neurology. Philadelphia: F. A. Davis. Mork. S. J.. Lindcgaard, K . , Halvorsen, T. B., Lehmann, E. H., Solgaard, T., Hatlevoll, R., Harvci, S., Ganz, J . (1985) ‘Oligodendroglioma: incidence and biological bchavior in ,a defined
. population.’ Journal of Neurosurgery, 63,
Visual Hallucinations after Acute Visual Loss in a Young Child
glioma) an 18-month course of chemotherapy was instituted. At the age of 2 % years his.optic discs were noted to be pale and his recognition visual acuity was 6/30 in both eyes. There were no other neurological abnormalities and he was otherwise well. CT scanning showed the tumour to have not increased in size. At the age of 3’1: years he was found to have a left temporal ficld loss, with no change in visual acuity. Over the next six months his vision gradually deteriorated until he had only light perception in his right eye and 6/60 in his left eye with severe peripheral field loss. A repeat C T scan revealed an increase in rhe size of the tumour and it was decided to recommence chemotherapy and debulk thc tumour. After surgery the child was torally blind; the postopcrative course otherwise was uneventful. One week after the operation he suddenly began to experience visual hallucinations: he saw people, including his brother and Santa Claus, animals and other familiar objects. The hallucinations moved around in both visual fields. They lasted for three days, abating only in sleep. No provoking factors were identified. There were no auditory, olfactory or tactile accompaniments. Initially he was frightened by the hallucinations, and became angry when told that they were imaginary. There was no previous history of visual hallucinations. The child’s mental status appeared normal apart from the visual hallucinations, and neurological and fundoscopic examinations were unchanged apart from the sudden visual loss. He was receiving no. medication and was afebrile. There was no evidence of ‘electrolyte imbalance o r other pituitary dysfunction. An electroencephalogram was normal and a repeat C T scan showed a significant reduction in the size of the tumour, but no new abnormalities.
C. P. White J. E. Jan
’
Visual hallucinations are common manifestations of toxic confusional states and psychoses. They may also arise secondary to lesions of the visual pathway anywhere from the eye to the cortex in otherwise healthy people. They are most commonly reported in older individuals with gradually deteriorating vision from a variety of causes, and are thought of as release phenomena (Cogan 1973). Rarely, they may be a manifestation of seizure activity in the occipital or temporal regions (Russell and Whitty 1955, Lance 1976). Hallucinations with visual loss have not been reported previously in young children.
Case report At the age of I 1 months the patient presented with a four-week history of nysragmus. Pregnancy and delivery had been normal, as had been his development until that time. Initial cxamination revealed the presence of an involuntary, bilateral, conjugate nystagmus of similar amplitude in both eyes. The horizontal nature of the nystagmus was maintained in upgaze. Neurological examination was unremarkable and there was no evidence of neurofibromatosis. A C T scan revealed the presence of a large suprasellar tumour extending posteriorly along the optic radiations. Following stereotactic biopsy (confirming the presence o f a low-grade optic
881-889. Ornitz, E. M. (1985) ‘Neurophysiology of infantile autism.’ Journal o/ rhe Amerjcan Acadenty of Child Psychiatry, 24, 25 1-262. Reiss. A. L., Fcinstein, C., Rosenbaum, K . N. (1986) ‘Autism and genetic disorders.’ Schizophrenia Bulletin, 12, 724-738. Tomira, T.. McLone, D. G . (1985) ‘Brain tumors during the first twenty-four months of life.’ Neurosurgery, 17, 913-919.
Discussion In 1769 Charles Bonnet published an account of the visual hallucinations experienced by his grandfather, an 89year-old man with severely decreased visual ‘acuity as a result of bilateral cataracts, who otherwise was in excellent physical and mental health. Since then there have been a number of other reports of such phenomena occurring in individuals, especially the elderly, in the absence of psychiatric disorder (DamasMora el al. 1982, Olbrich et al. 1987), and
m v.
m-
259
