To be published as part of the Novartis Foundation Symposium 251, “Autism: Neural Basis and Treatment Possibilities”, June 2002

The Amygdala, Autism and Anxiety

David G. Amaral, Ph.D.1,2 and Blythe A. Corbett, Ph.D.2

1Department of Psychiatry, Center for Neuroscience and California Regional Primate Research Center2The M.I.N.D. (Medical Investigation of Neurodevelopmental Disorders) InstituteUniversity of California, Davis, Center for Neuroscience, 1544 Newton Ct., Davis, CA, 95616

Number of pages: 20

Number of words: 3755

Number of tables: 0

Number of figures: 0

Running Title: Amygdala and Autism

Send correspondence and reprint requests to:

David G. Amaral, Ph.D.Center for Neuroscience1544 Newton CourtDavis, CA. 95616 USA

Telephone (530) 757-8813Fax (530) 754-7016e-mail dgamaral@ucdavis.edu

Abstract

Brothers (1990) has proposed that the amygdala is an

important component of the neural network that underlies social

cognition. And, Bauman and Kemper (1985) observed signs of

neuropathology in the amygdala of the postmortem autistic brain.

These findings, in addition to recent functional neuroimaging data,

have led Baron-Cohen et al. (2000) to propose that dysfunction of the

amygdala may be responsible, in part, for the impairment of social

functioning that is a hallmark feature of autism. Recent data from

studies in our laboratory on the effects of amygdala lesions in the

macaque monkey are at variance with a fundamental role for the

amygdala in social behavior. If the amygdala is not essential for

normal social behavior, as seems to be the case in both nonhuman

primates and selected patients with bilateral amygdala damage, then

it is unlikely to be the substrate for the abnormal social behavior of

autism. However, damage to the amygdala does have an effect on a

monkey’s response to normally fear-inducing stimuli, such as snakes,

and removes a natural reluctance to engage novel conspecifics in

social interactions. These findings lead to the conclusion that an

important role for the amygdala is in the detection of threats and

mobilizing an appropriate behavioral response, part of which is fear. If

the amygdala is pathological in subjects with autism, it may contribute

to their abnormal fears and increased anxiety rather than their

abnormal social behavior.

2

Introduction

In the best of biomedical research endeavors, there is a natural

symbiosis between basic, and often basic animal research, and

careful assessment of clinical populations. The issues raised in this

paper draw from efforts to establish the neurobiological basis of

primate social behavior, on the one hand, and attempts to determine

brain systems that are impacted in autism and lead to impairments of

social behavior, on the other hand. One effort has enormous potential

to inform the other. If for example, a neural system, let’s call it the

Social System, is established that underlies the various components

of social interaction, and given that impairments of social interaction

are a major deficit in autism spectrum disorders, then a reasonable

hypothesis might be that a region of primary brain pathology might be

in the Social System1. Conversely, if specific and reproducible areas

of brain pathology were identified in autism spectrum disorder, this

information might provide a useful heuristic as to which brain regions

might be components of the Social System.

Life, of course, is rarely so simple and autism is certainly one of

the most complex of neurological disorders. It is complex because it

has many diverse symptoms including social impairment, language

problems and motor stereotypies. These symptoms are observed

heterogeneously throughout the population that makes up the autism

spectrum. There are also a number of co-morbid conditions, such as

sleep disturbances, gastrointestinal distress and psychiatric

1 Of course, this is not necessarily the case. It could well be that autism is due to brain dysfunction(s) at a much more fundamental level of sensory or motor processing. And this dysfunction only manifests itself in complex situations such as social encounters.

3

symptoms including anxiety and obsessive-compulsive behavior. The

following is a short summary of the thought and experimental process

that we have followed - starting with the notion that the amygdala is a

fundamental component of the Social System and likely to be heavily

involved in the pathophysiology of autism - to our current view that

the amygdala is involved in detecting and reacting to environmental

threats. And, if the amygdala is impaired in autism, it may be more

responsible for alterations in fear and anxiety rather than social

behavior.

The Amygdala

The primate amygdala is a relatively small brain region located

in the temporal lobe, just anterior to the hippocampus. In the

macaque monkey it is approximately 0.6 cm3 in volume and in the

human it is about 3.0 cc3. The amygdala is comprised of at least 13

nuclei and cortical regions, many of which are partitioned into two or

more subdivisions. The amygdala has widespread extrinsic

connections including those with the neocortex, hippocampal

formation, cholinergic basal forebrain, striatum, hypothalamus and

brainstem. While neocortical inputs to the amygdala arise mainly from

higher order unimodal and polymodal association cortices,

projections back to the neocortex extend monosynaptically even to

primary sensory areas such as visual area V1. There is an extensive

network of intrinsic connections within the amygdala that generally

brings information from more laterally situated nuclei, such as the

lateral nucleus, to more medially situated nuclei, such as the central

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nucleus. The amygdala contains a plethora of neuroactive

substances and has some of the highest brain levels of

benzodiazepine receptors and opiates. Detailed descriptions of the

neuroanatomy of the amygdala can be found in Amaral et al. (1992).

One can conclude from the neuroanatomy of the amygdala that it is

privy to much of the sensory processing that occurs in the neocortex

and, that through its widespread efferent connections, it has the

ability to influence the activity of numerous functional systems that

range from elemental physiological processes such as heart rate and

respiration to the highest processes of perception, attention and

memory.

The Amygdala and Social Behavior

Several lines of evidence have indicated that the amygdala

plays an important role in socioemotional behavior. Macaque

monkeys with bilateral lesions that include the amygdala are typically

more tame than normal animals, demonstrate abnormal food

preferences and have alterations of sexual behavior (Brown and

Schafer 1887) (Kluver and Bucy 1938, 1939). Rosvold et al. (1954)

designed studies to explicitly evaluate changes in social behavior in

macaque monkeys following amygdala damage. They established

artificial social groups of male rhesus monkeys and studied the

dominance hierarchy that emerged. They then carried out two stage

bilateral destructive lesions of the amygdala of the most dominant

animal and studied the dominance hierarchy as the group

reorganized. They found that the lesions led to a decrease in social

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dominance with the lesioned animal typically falling to the most

subordinate position of the group.

A more extensive program of studies was carried out by Kling

and colleagues using both captive and free ranging nonhuman

primates (Kling et al. 1970, Kling and Cornell 1971) (Kling and Steklis

1976). Dicks et al. (1968), for example, retrieved rhesus monkeys

from social troops on the island of Cayo Santiago. These animals

were subjected to bilateral amygdalectomy and then returned to their

social groups. While it was difficult to follow the minute-to-minute

interactions of the lesioned animals, the typical finding was that they

were invariably ostracized and would often perish without the support

of the social group.

From the results of these and similar studies carried out by

several laboratories, Brothers (1990) formalized the view that the

amygdala is one of a small group of brain regions that form the neural

substrate for social cognition. This view predicts that the amygdala is

essential for certain aspects of the interpretation and production of

normal social gestures such as facial expressions and body postures.

It also predicts, consistent with the literature that damage to the

amygdala would invariably lead to a decrease in the amount or

quality of conspecific social interactions.

The Amygdala and Autism

In their seminal studies on the neuropathology of the autistic

brain, Bauman and Kemper (1985) noted that the medially situated

nuclei of the amygdaloid complex had clusters of small, tightly packed

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neurons that were not observed in control brains. The amygdala

neuropathology was only one area among many that included

alterations in the hippocampus, septum, cerebellum and other

structures. Unfortunately, these observations have not yet been

independently replicated. Neuroimaging studies have thus far

produced conflicting results on whether there is a gross change in the

volume of the amygdala. Abell et al. (1999) reported an increased left

amygdala volume in cases of autism and Asperger syndrome.

Howard et al. (2000) also reported an increased amygdala volumes in

both hemispheres of the brain in subjects with autism. In contrast to

these studies, Aylward et al. (1999), reported the amygdala to be

decreased in volume compared to age matched control cases.

Pierce et al. (2001) also reported amygdala volumes to be

significantly smaller. Thus, these studies appear inconclusive as to

whether there is a size difference in the autistic amygdala. Even if the

size was significantly different, it is unclear whether this would imply

better or worse function.

More suggestive evidence for a role of the amygdala in autism

comes from a variety of functional imaging studies. Individuals with

high functioning autism or Asperger syndrome showed significantly

less amygdala activation than control subjects during a task that

required them to judge what a person might be feeling or thinking

from images of their eyes (Baron-Cohen et al. 1999). A more recent

fMRI study, comparing adult males with autism to control subjects,

measured the neural activation in areas of the brain that are

associated with a social perception task (Ashwin et al. 2001).

Subjects were shown images of real faces that varied in intensity of

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facial affect from neutral expressions to extreme fear expressions, as

well as scrambled faces. The subject was simply required to press a

button every time they saw a picture on the screen. During this social

perception task, the subjects with autism showed less activation of

the amygdala and orbitofrontal cortex. Moreover, the subjects with

autism showed increased activity (implying greater reliance) on the

superior temporal gyrus and anterior cingulate cortex. These data

would appear to suggest that when normal subjects are carrying out

tasks that require social evaluation, the amygdala is activated. And

this activation is decreased in individuals with autism.

The Amygdala Theory of Autism

Based on these converging lines of evidence, Baron-Cohen et

al (2000) wrote a very compelling review that concluded, “The

amygdala is therefore proposed to be one of several neural regions

that are abnormal in autism.” An implication of the paper is that

pathology of the amygdala leads to an impairment in social

intelligence, which is a hallmark feature of autism. That the amygdala

might be at the heart of the pathophysiology of autism was also

suggested somewhat earlier by Bachevalier (1994, 1996) based on

observations of neonatal macaque monkeys who had been subjected

to bilateral medial temporal lobe lesions. Bachevalier described these

monkeys (at 6 months of age) as dramatically decreasing their social

behavior as compared to controls in dyadic social encounters with

conspecifics. The lesioned animals actively avoided social contacts

and had “blank, inexpressive faces and poor body expression (i.e.

8

lack of normal playful posturing) and they displayed little eye contact.

Furthermore, animals with early medial temporal lobe lesions

developed locomotor stereotypies and self-directed activities”

(Bachevalier 1994). Since selective lesions of the hippocampus did

not produce this pattern of behavioral alterations, Bachevalier

attributed them to damage of the amygdala.

The literature that figured prominently in the generation of the

amygdala theory of autism and the notion that the amygdala is

essential for normal social behavior was very influential on our own

program of studies aimed at unraveling the neurobiology of primate

social behavior. While we would have been delighted to have

generated data consistent with the hypothesis that the amygdala is

central to social behavior, the data we did generate has led us to a

distinctly different conclusion.

The Amygdala is not Essential for Social Behavior in the Adult Monkey

We have carried out a series of experimental studies to re-

examine the role of the amygdala in conspecific social behavior using

the rhesus monkey as a model system (Emery et al. 2001). Adult,

male rhesus monkeys with bilateral ibotenic acid lesions of the

amygdala, and age, sex and dominance matched control monkeys

were observed during dyadic interactions with “stimulus monkeys”

(two males and two females). This stereotaxic, neurotoxic lesion

technique has the merit of removing the neurons of the amygdala

while sparing fibers that pass through it. A variety of both affiliative

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(groom, present sex etc.) and agonistic, (aggression, displace etc.)

behaviors were quantitatively recorded while animals interacted in a

large (18ft X 7ft X 6.5ft) chain link enclosure. Each experimental

animal interacted with each stimulus animal for four, twenty-minute

periods in what we called the unconstrained dyad format. In what was

initially a very surprising observation, the amygdala-lesioned

monkeys generated significantly greater amounts of affiliative social

behavior towards the stimulus monkeys than the control monkeys.

Control monkeys, when they first met the stimulus monkeys,

demonstrated a typical and appropriate reluctance to engage in social

interactions. They appeared to go though a period of evaluation to

determine the intentions of the other animal. The lesioned monkeys,

in contrast, appeared to be socially uninhibited since they did not go

through the normal period of evaluation of the social partner before

engaging in social interactions.

The inevitable conclusion from this study is that in dyadic social

interactions, monkeys with extensive bilateral lesions of the amygdala

can interpret and generate social gestures and initiate and receive

more affiliative social interactions than normal controls. In short, they

are clearly not critically impaired in carrying out social behavior. We

would suggest that the lesions have produced a socially uninhibited

monkey since their normal reluctance to engage a novel animal

appears to have been eliminated. This, as well as evidence that the

amygdala-lesioned animals are not fearful of normally fear-inducing

stimuli such as snakes, has led us to the hypothesis that a primary

role of the amygdala is to evaluate the environment for potential

threats or dangers. Without a functioning amygdala, macaque

10

monkeys do not evaluate other novel conspecifics as potential

adversaries and whatever system(s) are involved in mediating social

interactions run in default mode of approach.

Early Amygdala Lesions do not Eliminate Social Behavior

One caveat of this conclusion that the amygdala is not essential

for social behavior is that these experiments were carried out in

mature monkeys. One might argue that while the amygdala is not

necessary for generating social behavior, perhaps it is essential for

gaining social knowledge. We have carried out a series of studies in

which the amygdala is lesioned bilaterally in primates at two weeks of

age (Prather et al. 2001). This is at a point in time when infant

macaque monkeys are mainly found in ventral contact with their

mothers and there is virtually no play or other types of social

interactions with other animals. We found that the interactions of the

lesioned animals with their mothers was similar to that of control

animals. Moreover, we found that, like adult animals with bilateral

amygdala lesions, they showed little fear of normally fear-provoking

objects such as rubber snakes. However, they showed increased

fear, as indicated by more fear grimaces and more screams during

novel dyadic social interactions. Most germane to the discussion,

however, is the finding that the lesioned animals generated

substantial social behavior that was similar to that generated by age-

matched controls. In a larger replication study that is currently under

way (Prather et al., unpublished observations 2002) the quality and

quantity of social interactions in a number of social formats is being

11

investigated and there may be subtle differences in these

parameters. However, the inescapable conclusion from observation

of these animals is that there are none that are markedly impaired in

generating species typical social behaviors such as grooming, play

and facial expressions. All of the animals appear to be visually

attentive of the other animals when they are involved in large “play

groups” comprised of 2 control animals, 2 animals with amygdala

lesions and 2 animals with hippocampal lesions as well as male and

female adult animals. And none appear to have developed motor

stereotypies despite the fact that they have now reached one year of

age.

The results from studies carried out both in adult and mature

rhesus monkeys with complete bilateral lesions of the amygdala have

forced us to consider the conclusion that the amygdala is not

essential either for interpretation or expression of species typical

social behaviors or for gaining social knowledge. If the amygdala is

not a central component of the Social System, it is unlikely that

pathology of it would lead directly to the impairments of social

behavior that are observed in autism.

Subject S.M.

There are relatively few human subjects who have bilateral and

discrete lesions of the amygdala. One outstanding exception is

patient S.M. who has been extensively studied by Adolphs and

colleagues (Adolphs et al. 1994, Adolphs et al. 1995). Patient S.M.

suffers from Urbach-Wiethe syndrome that has produced bilateral

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space occupying lesions of the amygdala. Interestingly, she is

impaired in her ability to identify fearful faces despite the fact that she

can reliably detect happiness and other emotions in faces. S.M. is

also unable to determine which individuals would typically be

considered untrustworthy based on their facial appearance (Adolphs

et al. 1998).

Despite these difficulties, patient S.M. leads a reasonably

normal life. She is capable of holding a job, has been married and is

raising children. One is impressed not so much with the deficits in this

subject who has no amygdala but rather by how intact is much of her

everyday behavior, including social behavior. A similar conclusion

can be drawn from patient H.M. who had bilateral temporal

lobectomies for intractable seizures. His surgery has completely

removed the amygdala and rostral half of the hippocampal formation

(Corkin et al. 1997). While H.M. is densely amnesic, he is

nonetheless capable of normal social interactions. And neither he nor

patient S.M. demonstrate typical autistic symptomatology. These

patients would seem to support the contention that the amygdala is

not essential for normal social behavior and that damage to the

amygdala does not necessarily lead to autistic behavior.

Anxiety in Autism

How does the concept of threat detection figure into the picture

of autism? In Kanner’s (1943) original report on autism, not only did

he describe social and language impairments, but he also highlighted

the anxious behavior exhibited in his initial sample of children. Fear of

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threatening events is considered a common experience among

primates and an adaptive response in humans (Reynolds and

Richmond 1994). Anxiety, on the other hand, is an emotional

response evoked when an individual perceives a situation as

threatening even in the absence of direct danger. We would suggest

that dysregulation of the amygdala might manifest itself in the

individual with autism as alterations either of fear or anxiety. Although

the presence of anxiety has been alluded to in descriptions (American

Psychological Association 1994) and classifications of autism

(Rescorla 1988, Wing and Gould 1979), the characteristics and

pervasiveness of this has not been well studied. However, recent

studies suggest that anxiety is an extremely common feature of the

autism spectrum disorders.

Muris et al. (1998) examined the presence of co-occurring

anxiety symptoms in 44 children with autism spectrum disorder. The

sample included 15 children with autism, and 29 with pervasive

developmental disorder-not otherwise specified (PDD-NOS). They

found that 84.1% of the children met criteria for at least one anxiety

disorder. In descending order, the percentage of children meeting

diagnostic criteria for an anxiety disorder were as follows: simple

phobia (63.6%), agoraphobia (45.5%), separation anxiety (27.3%),

overanxious (22.7%), social phobia (20.5%), avoidant disorder

(18.2%), obsessive-compulsive disorder (11.4%), and panic disorder

(9.1%). While the authors raised the caveat that anxiety symptoms

were assessed via parental interview, they noted that parents often

underreport internalizing symptoms, such an anxiety.

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More recently, Gillott et al. (2001) compared high-functioning

children with autism to two control groups including children with

specific language impairment and normally developing children on

measures of anxiety and social worry. Children with autism were

found to be more anxious on both indices. In fact, four of the six

factors on the anxiety scale were elevated with obsessive-compulsive

disorder and separation anxiety showing the highest elevations.

These studies do not provide much insight into the

pervasiveness of anxiety in autism. Both clinical and parental reports

indicate that not all children with autism demonstrate symptoms of

anxiety. The DSM-IV summarizes that children with autism may

exhibit “a lack of fear in response to real dangers, and an excessive

fearfulness in response to harmless objects” (APA 1994, p. 68). Wing

and Gould (1979) highlighted the heterogeneity in the occurrence of

anxiety in their classification system. Specifically, the active-but-odd

subtype tend to exhibit extreme reactions to social situations,

whereas the aloof subtype may be completely oblivious to

environmental changes. Rescorla (1988), conducted a factor and

cluster analysis using the Child Behavior Checklist (CBCL,

Achenbach 1991), a general instrument of childhood behavior, to

distinguish boys with autism from other disorders. Among many

differences, the analysis demonstrated that the more severe cases of

autism were distinguished from the milder ones based on the

presence or absence of anxiety.

The Amygdala and Anxiety

15

A number of recent studies have provided evidence that the

amygdala may be dysregulated in emotional disorders such as

anxiety and depression (Davidson et al. 1999). Tillfors et al. (2001),

for example, demonstrated increased blood flow in the amygdala in

social phobics anticipating a public presentation. Recently, Thomas et

al. (2001) used fearful faces as probes and demonstrated that the

amygdala of anxious children showed heightened activity in the

amygdala. De Bellis (2000) also showed that the right amygdala of

children with generalized anxiety disorder was larger than age

matched controls. These findings are consistent with the results of

our studies in nonhuman primates in that removal of the amygdala

produced animals that were less fearful of inanimate objects as well

as other monkeys.

Conclusions

The amygdala has been proposed to play an essential role in

the elucidation of normal social behavior. And, its dysfunction has

been proposed to play a role in the social pathology of autism.

Studies both in the rhesus monkey and data from human subjects

with bilateral lesions of the amygdala indicate that the amygdala is

not essential for many facets of normal social interaction. Rather, it

appears that the amygdala may have a more selective role in

detecting threats in the environment. If this proves to be correct, it

would be unlikely that dysfunction of the amygdala alone could

provide the substrate for the impairments of social interaction that are

a hallmark feature of autism. If, however, the amygdala is indeed

16

dysfunctional in autism, this could contribute to the abnormalities of

fear and anxiety that appear to be a common feature of autism. If this

were the case, one might expect the amygdala to be hyperfunctional

in autism rather than hypofunctional as predicted by the current

theories of the role of the amygdala in autism.

Acknowledgements

This original research described in this paper was supported, in part,

by grants from the National Institute of Mental Health and by the base

grant of the California National Primate Research Center. This work

was also supported through the Early Experience and Brain

Development Network of the MacArthur Foundation.

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