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J. Indian Assoc. Child Adolesc. Ment. Health 2016; 12(2):162-199

Review Article

The Neuropsychology of Autism – A Focus on Three Major Theories

Vanitha S Rao, Ashok V Mysore, Vijaya Raman

Address for correspondence: Dr. Vijaya Raman, Additional Professor of Clinical

Psychology, Department of Psychiatry, St. John’s Medical College Hospital,

Bengaluru. Email: vraman12@yahoo.co.uk

ABSTRACT

Autism is a developmental disorder that is biological in origin with a behavioural definition.

Numerous neuropsychological theories have been suggested to explain the triad of

impairments in autism. In this paper we have discussed the neuropsychology of autism with

emphasis on the three frequently researched cognitive theories related to the impairments in

Theory of Mind, Executive Function skills and Central Coherence. Each of the theories

explains some aspects of the disorder but it is in combination that their explanatory power

seems to increase. Focus of future research needs to be on the interactions between these

neuropsychological deficits.

Key words: autism, theory of mind, executive dysfunction, weak central coherence,

neuropsychology

Introduction

Autism is a developmental disorder that is characterized by socio-communication deficits and

restricted and repetitive repertoire of behaviours [1]. Its prevalence in India is not adequately

ascertained; some western reports suggest that it affects 1 in 68 individuals [2].

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Interest in understanding cognitive functions of individuals with autism has existed since

Kanner [3] reported them to be aloof, with poor communication skills but of normal

intelligence. Charman et al [4] have highlighted the challenges in establishing a cognitive

profile for autism. They consider the heterogeneous nature of the disorder and the difficulty

in obtaining large sample sizes for research as major impediments in this regard. A sound

neuropsychological theory clearly establishes the brain-behaviour connection. While many

theories have been proposed, there has been a dominance of research interest in three main

cognitive theories, Theory of Mind (ToM) [5], Executive Function (EF) [6] and Central

Coherence (CC) [7]. Although research often presents these three theories as separate

concepts they could be linked in ways that need investigation.

A seminal review paper [8] attempted to tease out the brain-behaviour-genetics connection in

autism. This paper proposed six broad autism phenotypic traits which is an admixture of

behavioural and cognitive characteristics. These traits are: a) face processing (b) social

affiliation (c) motor imitation (d) declarative memory/feature binding (e) executive function

and (f) language ability. Face processing and social affiliation are components underlying the

theory of mind. Motor imitation has been linked to language acquisition and social skill

development [9]. The declarative memory/feature binding trait has been linked to central

coherence and mapped to the prefrontal cortex region [10], the key region implicated in

executive function skills. These six traits are arguably linked to the three theories as they are

components/or derivatives of the theories.

Nearly 30 years after Ivar Lovaas [11] seminal paper received widespread interest

behavioural interventions still dominate as a possible solution to autism across the globe and

in India. Very little importance is given to neuropsychological findings. There is an urgent

need to highlight the importance of potential neuro-cognitive approaches to intervention. The

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three theories mentioned above have been the guiding principles for some intervention

models [12]. One paper that reviewed the three theories comprehensively [13] has suggested

that future research needs to focus on taking a more developmental and dynamic approach to

studying these theories as a multiple deficit account may help us understand autism.

Indian literature on autism includes references to neurobiology of autism [14] and reviews of

the Indian scene [15].

This article focuses on research in autism neuropsychology, discussing the three theories and

hints at the ways in which they have been incorporated in formulating intervention strategies.

Table No.1 lists broad aspects of cognition and functioning in the Autism Spectrum Disorders

(ASD)

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It is difficult to parse out deficits underlying general developmental delays from those

underlying specific autistic features. The cognitive profile in autism is extremely uneven

(Table 1). While language may be present in an individual, communication can be very

impaired. That a section of the autistic population is intelligent has always been apparent but

intelligence testing has remained a challenge. Research suggests better performance on the

Coloured Progressive Matrices (CPM); our own experience [29] has been that administering

the CPM to those attending special schools is difficult task. Only 20 of 28 children

considered high functioning by teachers could complete the CPM. All scored below average

compared to age matched controls. It is possible that only the more disabled children with

ASD enrol in training centers in India. Indian clinical scenarios too may show fewer children

with ASD in the normal intelligence range. On the other hand, Chakraborti and Fombonne

[24] (Table 1- column Intelligence) suggest that a wider range of able children with socio-

communicative limitations seek professional assistance in some western countries. Box No. 1

lists the definitions of the theories.

The term “theory of mind”(ToM)[5] refers to the ability to explain and predict

behaviour by hypothesizing on the thoughts, feelings and goals of partners.

Executive Functions (EF) has been defined as, “mental operations which enable an

individual to disengage from the immediate context in order to guide behaviour by

reference to mental models or future goals”.[6]

Frith used the term Central Coherence[7] (CC) to describe a characteristic of normal

information processing which is the tendency to draw together diverse information to

construct higher level meaning in context.

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The Major Cognitive Theories are described below:

I. Theory of Mind Deficits

Baron-Cohen and co-authors[5] had suggested that ToM deficits were caused by a defective

innate cognitive mechanism which in its intact form makes it possible to imagine what goes

on in the mind of others. The roots lie in infants’ strong interest in people as evident in their

attention to human faces and language and their ability to respond to affective expressions

within the first few months of life. Studies of early clinical markers of autism emphasize

problems with affect, orienting and responding to others and attention to language [30]. All

of these indicate profound innate difficulties in relating to other people. There have been

criticisms of the false belief task’s relationship to ToM[31]

Some key findings with regard to ToM have been highlighted in table 2.

The hypothesis of ToM deficits in autism and their relationship with difficulties in social

interactions and communication has been tested over the years. A study [48] conducted with

a test involving recognition of ‘faux pas’ in children showed that this ability developed with

age and that females did better than males. Some high functioning individuals with autism

did learn the ability to recognize ‘faux pas’ but still produced them.

Impaired ToM has been implicated in some forms of higher order social cognition such as

moral judgment[49] in high functioning children with autism (HFA). Deciphering mental

state information from expression in eyes [32] and voice [33] have been studied as

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components of ToM. More recent studies have raised doubts about the role of ToM with

regard to such prosodic perceptions. The term prosody includes the ability to appreciate

emotional content based on changes in acoustic parameters of language. Using vocal cues one

study [50] found that HFA children have subtle deficits in deciphering vocal cues compared

to normal controls. However, it also emerged that under high cognitive load, ASD subjects

were slower in recognising all vocal cues. They argue that the pattern of deficits seen is

inconsistent with the ToM account.

Literature has time and again reinforced the existence of the ToM but its relationship to the

core deficits of autism is still under investigation. The well known absence of adequate eye

contact in autism remains the core manifestation of ToM. The lack of interest that children

with autism show in focussing on others’ eyes could well be because they are unable to use

the information being conveyed by eyes leading to the social difficulties they face.

Theory of Mind & Its relation to Language Development

In the early years, language development and ToM seem to be very closely related. Joint

attention, cited as a stage in the development of ToM, is also known to be an essential

precursor for language development. But once language develops and ToM has reached the

stage of false belief understanding, the interface of language and ToM becomes a little

blurred [51]. In one longitudinal study [51], researchers gave false belief tasks, a working

memory task and language tasks tapping different aspects including syntax and semantics to a

group of typically developing preschool children. They found that the relationship between

language and ToM was bidirectional. Two recent studies [34] [35] using various tasks to

assess ToM deficits in ASD, typically developing children and those with deafness have

suggested that there is a different but consistent alteration of sequence of ToM development

in children with ASD. Specifically, they seem to fail the false belief based task even if they

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pass the hidden emotion task while higher proportion of children from other groups found

hidden emotions more difficult to pass. The second of these studies, while confirming the

findings, has introduced the ‘sarcasm task’ to complete a new ToM scale that can capture

developmental sequences and related variations in children with ASDs. This scale needs to be

validated in different contexts [34] [35]. The exact interface of language and ToM still

requires further study.

Theory of Mind and the Social Motivation Theory of Autism

Seyfarth & Cheney [52] have used the theory of natural selection to explain the evolution of

the ToM. They state that only those individuals, who are sufficiently motivated to attend to

others’ actions and behaviours, learn from it. These are individuals who seek the social

reward of “learning” from others. Another [53] model of social motivation suggests social

orientation and the need to be accepted in the social world as inherent in typically developing

individuals. Thus, while ToM plays an important role in social cognition in autism, it is

currently hard to overlook the argument that it appears to arise from more basic functions of

the brain such as face processing and social drives. It may be an intermediate cognitive

phenotype rather than a primary deficit.

Summary of ToM Deficits in ASD: Over 80% of children with autism fail ToM tasks

though these deficits are not specific to ASD. While the ToM can be used to explain some of

the deficits of autism in the areas of social relations, it fails to account for other features such

as - restricted and repetitive behaviours or savant abilities. The longitudinal sequence of

development of ToM ability may be different in ASD from that in hearing impaired children

or typical development. And it may be dependent on other deficits such as face processing,

social motivation and executive function.

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II. Executive Function

Executive Function (EF) is traditionally used as an umbrella term for functions such as

planning, working memory, impulse control, inhibition and shifting sets, as well as the

initiation and monitoring of action. These functions share the need to disengage from the

immediate environment in order to guide actions.

There are 3 separable but unified components of EF:

1) Attention control: selective attention and sustained attention.

2) Cognitive flexibility: working memory, attention shift, self-monitoring, and conceptual

transfer.

3) Goal setting: initiating, planning and organization, difficulties generating and

implementing strategies for problem solving, and strategic behaviour. Table 3 lists a few

studies relevant to ASD

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The first report of EF deficits in a case of residual state autism reported inflexible problem

solving strategies and perseveration [66]. The Cambridge Neuropsychological Test

Automated Battery (CANTAB) is a computer-administered set of tests developed to examine

specific components of cognition [67]. This was administered to individuals with autism and

normal controls, ranging from 6 to 47 years, matched on age, sex, and full-scale IQ.

Significant group differences were found in performance, with the autism group showing

deficits in planning efficiency and extra-dimensional shifting, relative to controls. Deficits

were found in both lower and higher-IQ individuals with autism across the age range.

Impairments did not predict autism severity or specific autism symptoms, but it was

correlated with adaptive behaviour.

Multitasking was studied in a group of HFA boys [68] by administering the Battersea

Multitask Paradigm along with matched controls. Multitasking involves the ability to

organize and execute different tasks along with a good working memory and all other

components of EF skills. Participants performed poorly compared to controls. Trying to

control for Intellectual Delays and its impact on EF in children with ASD, a recent study has

suggested that impaired flexibility and efficient planning may be more central to ASD as they

are present in children with and without Intellectual Delay [69].

EF and Language Ability

Executive dysfunction and its relation to language ability in verbal school age children with

autism has been examined [70] [71]. Children with autism exhibited deficits across all

domains of EF that were assessed - working memory, inhibitory control and planning.

Children with autism were less developed than the controls in their language skills, but

correlational analyses revealed no specific association between language ability and

executive performance in the autism group. In contrast, executive performance was positively

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correlated with language ability among controls. This pattern of findings has been interpreted

to mean that executive dysfunction in autism is not directly related to language impairment

per se. There may be an executive failure in the use of language for self-regulation [70][71].

EF & Adaptive Behaviour:

Gilotty et al [72] examined the relationship between EF and adaptive behaviour in children

with ASD. 30 boys and 5 girls (ages 6-17), with a full scale IQ of at least 70 participated in

the study. Two parent questionnaires were used – The Vineland Adaptive Behaviour Scales

and the Behaviour Inventory of Executive Functions. EF impairments were strongly

associated with the deficits in communication, play and social relationships found in children

with autism. The impact of executive impairments on adaptive behaviour and real world

functioning has been seen to increase with age and is more prominent when the ASD subjects

are likely to foray into employment [73]. Yet another recent study that examined the

development of EF and autistic symptoms in HFAs over three points in time confirmed the

impact of EF on adaptive behaviours [74].

EF & Restricted Behaviours:

The relationship between EF and the restricted & repetitive symptoms of Autism was

examined in 17 adults and 17 controls [75]. Cognitive flexibility, working memory and

response inhibition (EF components) were highly related to the restricted and repetitive

symptoms of Autism. Impaired response generation and behavioural inhibition have been

proposed as potential explanations for stereotypical behaviours [76].

ToM & EF

A cross cultural study with Chinese and US preschoolers using EF and ToM tasks was

conducted to determine the relationship between ToM and EF [77]. The EF tasks carried out

were primarily related to inhibition control. The Chinese children out-performed the US

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children on all measures of EF but were not similarly advanced in ToM reasoning.

Nonetheless individual differences in EF predicted ToM reasoning in both cultures

demonstrating that executive functioning is necessary for development of the ToM.

Subsequently their independent impact on adaptive behaviours varies.

Prospective memory is the ability to carry out a task in the future and it can impact on

adaptive functioning. Exploring the independent contributions of EF and ToM deficits to time

based and event based prospective memory tasks, researchers [58] reported that time based

prospective memory deficits are more commonly seen in HFA and ToM had a significant

association with such deficits. Cognitive flexibility did not seem to play a role in this study.

Another recent study that examined the development of EF and autistic symptoms in HFAs

over three points in time confirmed the impact of EF on adaptive behaviours [74].

Summary of Executive Function: Impairments in EF abilities have been widely reported in

children with autism and appear to account for many of the features including the varied

adaptive behaviour profile and restricted, repetitive behaviours. On the other hand, these

deficits fail to show significant relationship with perceptual characteristics of individuals with

autism. To highlight the complexity, even measures of Central Coherence (discussed later)

and restricted and repetitive behaviours themselves have not always related significantly with

each other [78]. Also, executive dysfunction is not specifically associated with autism. It

would be interesting to study why the same fundamental deficit in say, ADHD, leads to

different impairments as in autism. Happe et al [79] while examining the EF profiles among

autism, ADHD and typically developing children found the EF deficits to be less severe but

persistent in autism than ADHD. They report that children with ADHD had more inhibitory

problems while those with autism had difficulties in response selection. However, other

researchers [80][81] have concluded that EF deficits are more profound and generalized in

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autism. Children with autism show significant deficits in vigilance when compared to

typically developing children. They also had significant deficits in response inhibition,

cognitive flexibility and working memory when compared with ADHD and typically

developing children [80].

III Central Coherence (CC)

Frith [7] used the term CC to describe a characteristic of normal information processing

which is the tendency to draw together diverse information to construct a higher level

meaning in context.

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In order to directly examine the ability to integrate elements into a whole image, adults

with ASD and normal adults were asked to name a familiar object moving behind a

narrow vertical slit[94]. Pictures were first presented behind the slit at a fast and a slow

speed. Subsequently whole pictures were presented in front of the slit at the fast speed

(full viewing). Both groups were good in the full viewing condition, but those with

autism were significantly poorer in slit viewing. The results were taken to indicate that

individuals with ASD have a deficit in integrating pieces of information received over

time into the whole picture.

The notion of weak central coherence (WCC) refers to a decreased ability in global

processing and an enhanced ability with processing local detail. According to Happe [95]

spared or superior functioning in certain areas cannot be explained by a general deficit;

instead we should consider that individuals with autism have a distinctive cognitive style

that leads to peaks and troughs in performance.

CC & Language Skills:

Linguistic processing in normally intelligent adults with ASD has been explored to test

whether local coherence is impaired [96]. Three tests were used: 1) The Homograph Test

2) Local Coherence Inferences Test and 3) Ambiguous Sentence Test. Results suggest

that individuals on the autism spectrum are impaired in achieving local coherence and

they have a preference not to strive for coherence unless instructed to do so or unless they

make a conscious decision to do so. CC ability appears to have an impact on language

abilities in children with autism.

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CC & Savant Skills:

The word Savant refers to individuals who despite having severe intellectual impairments

nevertheless show extraordinary skills in a particular cognitive area. Approximately 10%

of individuals with autism have Savant skills thus greatly enhancing its diversity. Half of

all savant people have autism [97]. Detail focussed attention and memory are said to

predispose an individual to special talents both in the general population and in autism.

Since such a large proportion of individuals with savant skills have autism, there is a

strong likelihood of some commonality at the neuronal level and a further understanding

of savant skills could lead us to a better understanding of CC and vice versa.

Summary of Weak Central Coherence theory: The Weak CC theory can be used to

explain the perceptual characteristics of autism. It can be stretched to account for the

savant abilities as well. It may be mentioned here that one study found that better CC in

early years resulted in better ToM while a reciprocal effect was not found [98]. Another

study [99] on typically developing preschoolers found one aspect of CC (visual-spatial)

to be related to different dimensions of executive control. However Booth & Happe

[100], while developing a tool to measure CC through language, found no association of

CC with EF suggesting that the association becomes weaker in the higher order

functioning of language.

Summary of Neuropsychological Findings

While the importance of ToM and its impact on social-communication cannot be ignored,

there seems to be a large body of research pointing to EF as important to understanding

autism. It is not clear how CC factors into everyday adaptive behaviour, although its role

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in stereotypical and restricted behaviour routines, seem to have good support. It appears

that an understanding of the impact of each of the three deficits on the other two remains

inadequate. One significant longitudinal study [98] attempted to document the impact of

each of these theories on the developmental outcome in high functioning children with

autism. Better CC appears to relate to better ToM though not vice versa. Early EF skills

predicted ToM skills while the reverse was not true. An interesting finding was that while

EF skills and ToM improved with time, performance on CC remained constant. One

report [101] had also found that one aspect of CC (integration) to be related to one aspect

of executive control but the direction of the effect was uncertain.

A growing number of studies looking at the factor structure of autistic traits seem to

indicate the presence of a general autism factor (GAF) with or without a social

communication factor [102]. Neuropsychological explorations into the integrity of the

GAF at a trait level have not been optimally carried out. One recent study [103] has

however cautioned with regard to assumptions underlying such studies and the nature of

broader phenotype measures used. Any neuropsychological model also needs to explain

the global cognitive heterogeneity in autism. On the other hand, some of the known

neuropsychological models are already being applied in interventional research.

Outcomes of such research may further help understand the complex interplay between

various neuropsychological aspects.

Case control studies and neuro-imaging studies to an extent have brought some validation

to the ToM and EF deficits while fMRI studies and reading comprehension have been

used to validate the construct of weak central coherence. The figure below summarizes

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what we know about autism neuropsychology today.

Figure 1: Summary of Autism Neuropsychology

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Significance of Neuropsychological Findings in Autism Intervention

Intervention in autism has traditionally relied on behavioural approaches but in light of

what we know today, we would do well to consider methods which will enable us to

overcome or otherwise compensate for these neuropsychological deficits/differences.

Lovaas’ sensational results created considerable interest in behavioural intervention but

subsequent researchers were unsuccessful in replicating Lovaas’ study [104].

“What Works Clearing House” (WCC) [105] is a report produced by the US Department

of Education on the various effective intervention strategies available. The WCC in 2010

found that the Lovaas Model had positive effects on cognitive development, but did not

have any discernable effect on language and social development or functional abilities of

children with autism. A systematic review of interventions for ASD found “No definitive

evidence suggesting superiority of Lovaas over other active interventions”[106]. While

we are as yet unable to change the way the brain is wired in autism, we could adapt the

way in which we provide inputs and also help support the outputs in order to

accommodate to the differences in the wiring[107]. The Early Start Denver Model

(ESDM) [108] is an intervention model that integrates the behavioural and

developmental-relationship based approach. A randomized control trial using the ESDM

showed that children with autism maintained their rate of growth in adaptive behaviour

after two years of intervention. This promising approach strengthens the importance of

understanding and using neuropsychological approaches to intervention.

Conclusion

Each of the three theories considered here seem to explain some aspects of autism but it

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is in combination that their explanatory power seems to increase. Language abilities and

EF are necessary for ToM development which in turn is required for narrative abilities to

enable spontaneous conversation. CC in turn is necessary to understand the bigger

picture.

No single deficit may explain all the core symptoms of autism, if one goes by reports of

the less extreme forms of these behaviours being inherited almost entirely independently

of each other within the general population [109]. However, controversies continue about

single core deficit vs. multiple deficits [110, 111]. If the autistic traits show confluence

into single factors in the general population, which are also continually distributed [102],

one tends to imagine that interactions amongst the deficits are more likely. The

possibility of autism being a unitary disorder has been under query for some time now

[112]. If multiple deficits can lead to myriad manifestations of the disorder, intervention

techniques may vary depending on the deficits in each case. The focus of future research

needs to be on the interaction amongst various neuropsychological deficits and their

implications for intervention strategies at different age levels.

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Appendix

Box 1: Definition of Key terms

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Ms. Vanitha S Rao, PhD Scholar; Dr. Ashok V Mysore, Professor; Dr. Vijaya Raman,

Additional Professor of Clinical Psychology, Department of Psychiatry, St. John’s

Medical College Hospital, Bengaluru.