Revision date: 4 April 2016

A Failure of ‘Theory of Mind’ in Brain Injury & Autism

Alan Challoner MA MChS

Theory of Mind

This rather abstract title refers to the ability (or lack of it) to understand the desires, beliefs
and intentions of others. This capacity is usually acquired gradually by children as they pass
from age three to the age of seven. It is one of most important developments in early
childhood social cognition. 1, 2 It also includes the ability to attribute mental states — such
as pretending, knowledge, etc. — to oneself and others and to understand that others
have beliefs, desires, and intentions that are different from one's own. Social cognition is at
the heart of children’s ability to get along with other people and to see things from their
point of view. We use theory of mind to explain our own behaviour to others, by telling
them what we think and want, and we interpret other people’s talk and behaviour by
considering their thoughts and wants.

Theory of mind develops gradually, with intuitive social skills appearing in infancy and then
reflective social cognition developing during the toddler and preschool years. Three-year-
olds know that different people may want, like and feel different things. By age 4 or 5,
children know that people may think different things. They understand that sometimes a
person may believe something that is not true but, in that case, what the person does or
says is based on a false belief.

There are differences in the rate of typical development that partly depend on factors in
the environment, such as family talk and disciplinary strategies, interaction with siblings,
story books and pretend play; as well as factors in the child, such as language and
cognitive control abilities. There are consequences to theory of mind development that
are seen in children’s social competence and success in school.3
The presumption that others have a mind is termed a theory of mind because each human
can only intuit the existence of his or her own mind through introspection, and no one has
direct access to the mind of another. It is typically assumed that others have minds by
analogy with one's own, and based on the reciprocal nature of social interaction, as

1 Flavell JH, Miller PH. Social cognition. In: Kuhn D, Siegler R, eds. Cognition, perception and
language. 5th ed. New York, NY: Wiley; 851-898. Damon W, gen ed. Handbook of child
psychology; vol. 2; 1998.
2 Harris PL. Social cognition. In: Kuhn D, Siegler RS, eds. Cognition, perception, and language.
6th ed. Hoboken, NJ: Wiley; 2006: 811-858. Damon W, Lerner RM, gen eds. Handbook of child
psychology; vol. 2; 2006.
3 Astington JW & Edward MJ. The development of theory of mind in early childhood. In:
Tremblay RE, Barr RG, Peters RDeV, Boivin M, eds. Encyclopedia on Early Childhood
Development [online]. Montreal, Quebec: Centre of Excellence for Early Childhood
Development; 2010:1-6. Available at: http://www.child-
encyclopedia.com/documents/Astington-EdwardANGxp.pdf. Accessed [29 October 2012].

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observed in joint attention,4 the functional use of language,5 and understanding of others'
emotions and actions.6

The appreciation of others’ thoughts, feelings, knowledge, and wishes is essential for
competent communication. Without a theory of mind, in communication with others, we
may give too much information, or too little; we may hurt their feelings, confuse them, or
bore them. With a theory of mind, we can judge what others need and want to know.7

Saxe et al in their study8 showed that a region of human temporo-parietal junction (TPJ) is
selectively involved in reasoning about the contents of other people’s minds. Regions near
the TPJ have preferential responses to human faces9 , bodies 10 and biological motion11 .
Researchers are therefore examining these areas to try and establish if damage to them will
indicate or even cause autism or autistic spectrum disorder. (See below)

In everyday life, human mental activity often happens at the moment of social interaction
among two or multiple persons instead of only one-person. Understanding the interactive
mind of two- or multi-person is more complex and higher than understanding the single-
person mind in the hierarchical structure of theory of mind. Theory of mind processing
depends upon at least two kinds of representation: representation of another person and a
representation of that other person's mental state. While representation of a person is a
likely prerequisite for theory of mind, achieving a representation of another's mental state is
the core feature of theory of mind12 . Reading the single mind and reading the interactive
mind both need the representation of person.

Theory of Mind and Autism

Autism, archetype of the autistic spectrum disorders (ASD), is a neuro-developmental

disorder characterised by socially aloof behaviour and impairment of language and social
interaction. Its prevalence has surged in recent years. Advanced functional brain imaging
has confirmed pervasive neurologic involvement. In addition to the central coherence
paradigm, autism has been variously characterized as a deficit of executive function 13,

4 Baron-Cohen, S. Precursors to a theory of mind: Understanding attention in others. In A.

Whiten (Ed.), Natural theories of mind: Evolution, development and simulation of everyday
mindreading (pp. 233-251). Oxford: Basil Blackwell; 1991.
5 Bruner, J. S. Intention in the structure of action and interaction. In L. P. Lipsitt & C. K. Rovee-
Collier (Eds.), Advances in infancy research. Vol. 1 (pp. 41-56). Norwood, NJ: Ablex Publishing
Corporation; 1981.
6 Gordon, R. M. 'Radical' simulationism. In P. Carruthers & P. K. Smith, Eds. Theories of theories of
mind. Cambridge: Cambridge University Press; 1966.
7 Miller, CA. Language and Theory of Mind: Developmental Relationships Between Language
and Theory of Mind. American Journal of Speech-Language Pathology _ Vol. 15 _ 142–154 _
May 2006.
8 Saxe, R. & Kanwishera, N. People thinking about thinking people: The role of the temporo-
parietal junction in “theory of mind”. NeuroImage 19 (2003) 1835–1842.
9 Hoffman, E.A., Haxby, J.V., Distinct representations of eye gaze and identity in the distributed
human neural system for face perception. Nat. Neurosci. 3, 80–84; 2000.
10 Downing, P.E., Jiang, Y., et al., A cortical area selective for visual processing of the human
body. Science 293, 2470–2473; 2001.
11 Grossman, E., Donnelly, M., et al., Brain areas involved in perception of biological motion. J.
Cogn. Neurosci 12, 711–720; 2000.
12 Leslie A. M. “Theory of mind as a mechanism of selective attention,” in The New Cognitive
Neurosciences, 2nd Edn, ed. Gazzaniga M., editor. (Cambridge: MIT Press; ), 1235–1247; 1999.
13 Ozonoff, S; Pennington, B & Rogers, SJ. Executive function deficits in high-functioning autistic
individuals: relationship to theory of mind. J Child Psychol Psychiatry; 32:1081–1105; 1991.

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complex information processing14, theory of mind 15, and empathy16. Some of the most
characteristic brain dysfunctions that are found in autism affect the amygdala and its
connections to the prefrontal cortex.

The connections of frontal cortex with other brain areas are of considerable significance
especially for understanding the neural basis of prefrontal psychological function. The
prefrontal cortex receives direct or indirect input from most ipsilateral cortical areas and
from the opposite hemisphere via callosal connections. In addition, prefrontal cortex
receives strong input from a number of significant subcortical sources:

1. The limbic system,

2. The reticular system,

3. The hypothalamus, and

4. Neurotransmitter systems.

The pre-frontal cortex is the only cortical area that receives strong sensori-motor, limbic, and
reticular input. Additional input of hypothalamic and autonomic data and the effects of
many neurotransmitters place prefrontal cortex in a strong position to monitor both intrinsic
and extrinsic stimuli and to exert regulatory control of brain functions.

Behavioural functions performed by the prefrontal cortex have proved difficult to delineate.
To date, almost all information has been derived from behavioural aberrations seen
following frontal brain damage. In the past several decades some psychological tests
aimed directly at the assessment of prefrontal function have been devised and, more
recently, psychological testing has been combined with functional brain imaging
techniques to provide valuable insights. In general, however, psychological tests of
prefrontal function demand inferences from data obtained through primary sensori-motor
functions, which of themselves may be impaired. A second problem in studying prefrontal
function is a lack of clearly delineated neuropathology. 17
Individuals with autism tend to have extreme difficulty learning from experience and
modifying their behaviour to accommodate varying situations. 18 Coping with the
unpredictability of the social world is especially demanding, even overwhelming, for adults
with autism; associated anxiety exacerbates the problem. (Bryson, et al; Idem) Adult
individuals with autism have life outcomes that range from complete dependence to
(rarely) successful employment.19

The most recently favoured hypothesis for social cognitive impairment in autism features
theory of mind.20 It suggests that autistics fail to appreciate the representational theory of

14 Minshew, NJ; Goldstein, G & Siegel DJ. Neuropsychologic functioning in autism: profile of a
complex information processing disorder. J Int Neuropsychol Soc 3:303–316; 1997.
15 Baron-Cohen S; Leslie AM. & Frith U. Does the autistic child have a “theory of mind’’?
Cognition 21:37– 46; 1985.
16 Baron-Cohen, S. The extreme male brain theory of autism. Trends Cogn Sci 6:248 –254; 2002.
17 For a fuller explanation see: Challoner, A. A study of a single case of atraumatic brain injury in
a five-month old infant and arising from the administration of the DPT Vaccine in 1960;
https://www.scribd.com/doc/223345698/A-Study-of-a-Single-Case-of-Atraumatic-Brain-Injury-
MDL
18 Bryson SE, Smith IM. Epidemiology of autism: prevalence, associated characteristics, and
implications for research and service delivery. Ment Retard Dev Disabil Res Rev 1998;4:97-103.
19 Persson B. Brief report: A longitudinal study of quality of life and independence among adult
men with autism. J Autism Dev Disord 2000;30:61-66.
20 Baron-Cohen S, Leslie AM, Frith U. 1985 Idem.

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mind and instead think of mind on too literal a basis. For example, the autistic child shown
a milk carton filled with paper clips may conclude the carton really was manufactured to
carry paper clips. Children normally can correct such false beliefs by the time they reach
age four. Children with ASD typically do not pass this stage until their verbal mental age is
at least eight years.

This involves a child in constant tracking. A child does something to activate a response
from someone's line of sight. For instance, they may look at what mother is looking at and
then look at her. Or a child might do something to catch mother's vision — wave a toy in
front of her, smile and see if she focuses upon it and them. Behavioural sonar thus
increasingly leads to an awareness of the existence of mental contents. Interestingly,
theory of mind seems developed most in those with the greatest opportunity to socialise
with others — members of large families.21

The ability to attribute mental states to others pervades normal social interaction and is
impaired in autistic individuals. Difficulty in understanding other minds is a core cognitive
feature of autism spectrum conditions. The theory of mind difficulties seem to be universal
among such individuals. (Baron-Cohen, 1991, idem)

In a positron emission scan study of normal volunteers, performing a ‘theory of mind’ task,
there was an associated activity in left medial prefrontal cortex. These patients showed
significant activation of a neighbouring area of left medial prefrontal cortex, when
processing theory of mind stories, however. Controls also showed activation in this area,
but to a far lesser extent. This partial overlap between the results from the two groups
suggests that the Asperger subjects’ mentalizing performance was subserved by a brain
system in which one key component was missing.22 While frontal lobe dysfunction has been
suggested for people with autism and Asperger syndrome,23, 24 the Happé findings suggest
the need for more specific task analysis of executive functions and a fractionation of the
possible components and brain pathways involved.
Boddaert and Zilbovicius also described other types of activation studies with autistic
children and adults. 25 All the PET studies are consistent with disorganised establishment of
neural circuits. Baron-Cohen and colleagues26 tested the social intelligence (theory of
mind) of autistic adults. Two sets of images were presented: (1) photographs of eyes, for
the subject to guess whether each was a man or a woman and (2) photographs of people,
for the subject to describe the mental state of the person in the photograph. The non-
autistic control subjects activated both the fronto-temporal neocortical regions and non-
neo-cortical regions, including the amygdala, hippocampus, and striatum. The autistic
subjects activated the frontal neocortex less extensively, and failed to activate the
amygdala. In other studies, autistic subjects failed to activate a cortical face area when
attempting to assess facial expressions. The amygdala and cerebellum were not activated
during processing of emotional facial expressions.

In summary, state-of-the-art functional brain imaging has established that autistic

individuals exhibit abnormal temporal lobe function. Dysfunctional connections between
these regions and the fronto-parietal zones could explain the cognitive abnormalities; to

21 Perner, J., Ruffman, T., & Leekam, S. R. (1994). Theory of mind is contagious: You catch it from
you sibs. Child Development, 63, 1228-1238.
22 Happé, F.; Ehlers, S.; Fletcher, P.; Frith, U.; Johansson, M.; Gillberg, C.; Dolan, R.; Frackowiak, R.
& Frith, C. ‘Theory of mind’ in the brain. Evidence from a PET scan study of Asperger
syndrome. NeuroReport 8, 197–201; 1996.
23 Ozonoff S, Pennington BF and Rogers SJ. J Child Psychol Psychiat 32, 1081–1106 (1996).
24 Hughes C, Russell J and Robbins TW. Neuropsychologia 32, 477–492; (1994).
25 Boddaert N, Zilbovicius M. Functional neuroimaging and childhood autism. Pediatr Radiol
2002;32:1-7.
26 Baron-Cohen S, Ring HA, Wheelwright S, et al. Social intelligence in the normal and autistic
brain: an fMRI study. Eur J Neurosci 1999;11:1891-1898.

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the limbic system, the emotional abnormalities; and to the auditory regions, the sensory
perception abnormalities. Functional imaging detected abnormal activation patterns
sufficient to suggest more or less widespread disorganisation of cortical networks in the
autistic brain.27

Most experts agree the neurological problems seen in autism seem to stem, not primarily
from the senses, but from interpretation of the world.28 When normal people view an array
of objects, for example, they infer social relationships among the objects. Rather than see
a room, they see individual details within it. Autistic people tend to see shapes and objects
as isolated. They also have trouble interpreting faces, sometimes gazing at the mouth
rather than the eyes, as normal people usually do. The autistic child would more often
describe his father as a man who is tall and wears glasses, rather than as his father who is
kind and works hard. (Stokstad, 2001 Idem))

Theory of Mind and Brain Damage

Lack of a theory of mind has important knock-on effects upon emotions. The cerebellum is
linked to the hypothalamus, amygdala, hippocampus, anterior cingulate and prefrontal
cortex. 29,30,31,32,33 They make up our limbic system — the part of the brain which creates
our emotions. During development this emotional processing needs to become socialised
and that needs the brain to associate with other people's responses, particularly as shaped
by their minds. What is the point of crying if we cannot connect with a meaning for those
tears and provide or receive a comfort? Why should we seek to enjoy doing something
with another if we cannot link this with the pleasure of their responses back to us? Infants
need these connections if they are to grow emotionally.
If the prefrontal cortex is damaged by toxins there may be nociceptive discharges34
evoked and these are conceivably involved in the affective rather than the sensory-
discriminative responses. Monosynaptic projections from the basolateral nucleus of the
amygdala to the prefrontal cortex are known to produce long-lasting synaptic plasticity35.
If the prefrontal cortex is damaged in a way that interferes with the synaptic plasticity then
there may be resulting abnormalities in the amygdala and the hippocampus and these
may mimic some aspects of autistic spectrum disorder and thus these may be associated
with loss of acquired motor, communication, and social skills. It has also been discovered

27 Kidd, PM. Autism, an extreme challenge to integrative medicine. Part 1: the knowledge
base. Altern Med Rev. 2002 Aug;7(4):292-316.
28 Stokstad E. Development. New hints into the biological basis of autism. Science;294:34-37;
2001
29 Heath, R., & Harper, J. Ascending projections of the cerebellar fastigial nucleus to the
hippocampus, amygdala, and other temporal lobe sites. Experimental Neurology, 45, 268-
287.;1974.
30 Haines, D., May, P., & Dietrichs, E. Neuronal connections between the cerebellar nuclei and
hypothalamus in Macaca Fascicularis: Cerebello-visceral circuits. Journal of comparative
neurology, 299, 106-122; 1990.
31 Supple, W. J. Hypothalamic modulation of Purkinje cell activity in the anterior cerebellar
vermis. NeuroReport, 4, 979-982; 1993.
32 Vilensky, J. A., & Van Hoesen, G. W. Corticopontine projections from the cingulate cortex in
the rhesus monkey. Brain Research, 205, 391-395; 1981.
33 Schmahmann, J. D. The cerebellum in autism: Clinical and anatomic perspectives. In M. L.
Bauman & T. L. Kemper, (Eds.), Neurobiology of autism, pp 195-226, Baltimore, ML: John
Hopkins University Press; 1994.
34 A tissue damaging event
35 The ability of the connection, or synapse, between two neurons to change in strength in
response to either use or disuse of transmission over synaptic pathways

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that injuries of this type may bring about cognitive abnormalities. Hippocampus-
dependent spatial memory, contextual fear memory, and social memory may also be
significantly impaired. 36

A child will be socially blinded if it lacks the ability to see how its stimulation of others’ minds
makes return responses. People might be responding to their attempts to interest and
interact with them, but their brains would be indifferent to their returning behavioural
echoes. As a result they would be unable to use feedback to give them a sense of their
presence in the world. They will, as a result, stop seeking social responses, becoming to the
outside world, remote and unaffectionate. Thus cerebellar circuits and their links with the
rest of the brain which enable tracking are essential: it is they that give us our interface with
human life, and so let us emotionally grow up as social beings.

Denis et al studied theory of mind in children with traumatic brain injury (TBI) and age- and
gender-matched children with orthopaedic injuries (OI), using a new three-frame Jack and
Jill cartoon task that measured intentional thinking separate from contingent task demands.
In the key theory of mind trials, which required intentional thinking, Jack switched a black
ball from one hat to another of a different colour, but Jill did not witness the switch; in the
otherwise identical non-theory of mind trials, the switch was witnessed. Overall accuracy
was higher in children with OI than in those with TBI. Children with severe TBI showed a
larger decline in accuracy on theory of mind trials, suggesting a specific deficit in theory of
mind among children with severe TBI. Accuracy was significantly higher on trials following
errors than on trials following correct responses, suggesting that all groups monitored
performance and responded to errors with increased vigilance. TBI is associated with
poorer intentional processing in school-age children and adolescents relative to peers with
OI; furthermore, children with TBI are challenged specifically by intentional demands,
especially when their injury is severe.37

Play behaviours were tested by Pletnikov et al using the ‘intruder-resident’ paradigm, with
social isolation of residents for six days prior to testing. Four experimental pairings of
infected (BDV) and uninfected (NL) rats were studied as follows: NL–NL; NL–BDV; BDV–NL;
and BDV–BDV (the first member is the resident, the second member is the intruder).
Observation of social activities was carried out for 10 min on two consecutive days. Non-
social exploratory activity (e.g. ambulation and rearing) was similar in BDV and NL residents.
Duration of non-play social investigation (e.g. sniffing, approach, and follow) was higher in
BDV residents as compared to NL residents when tested on the first test day. On the
second day, all rats showed similar level of non-play social interaction. When confronted
with NL intruders, NL residents exhibited significantly more play behavior compared to the
NL–BDV, BDV–NL and BDV–BDV pairs, when play behavior was measured by the number of
`pins'. Moreover, irrespective of a type of intruder, NL residents demonstrated higher play
soliciting behavior than BDV residents, indicating attenuated readiness to play in BDV-
infected rats. The number of pins and play solicitations in BDV–NL pairs significantly
increased over the two days of testing, while play activity in NL–BDV pairs declined on the
second test day. This pattern suggests that the degree of social reinforcement on the first
day of testing affected the level of play on the second day. These data demonstrate
deficits in play behavior and other social interactions following BDV-associated
developmental brain injury, thus supporting the value of the neonatally BDV-infected rat as
an animal model of autism.38

36 Moretti, P.; Levenson, JM.; Battaglia, F.; Atkinson, R.; Teague,R.; Antalffy, B.; Armstrong, D.;
Arancio, O.; Sweatt, JD. & Huda Y. Zoghbi1, HY. Learning and Memory and Synaptic Plasticity
Are Impaired in a Mouse Model of Rett Syndrome. The Journal of Neuroscience, January 4,
2006 • 26(1):319 –327 • 319
37 Dennis M, Simic N, Gerry Taylor H, Bigler ED, Rubin K, Vannatta K, Gerhardt CA, Stancin T,
Roncadin C & Yeates KO. Theory of mind in children with traumatic brain injury. J Int
Neuropsychol Soc. 2012 Sep;18(5):908-16.
38 Pletnikov, MV.; Rubin, SA.; Vasudevan, K.; Moran, TH. & Carbone, KM. Developmental brain
injury associated with abnormal play behavior in neonatally Borna disease virus-infected

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The cognitive impairments of patients with prefrontal damage are apparent in a variety of
tasks. The domains affected include: complex motor behaviour, planning and sequencing,
attention, memory, and language. Often patients can perform well on standard tests of
intelligence but fail miserably in less constrained real-life situations calling for planning and
flexibility. 39

There are important aspects of brain pathology that can be common features in those with
classical autism, autistic spectrum disorder and brain injury that affects particular areas. So
clear has this become that there may be a further connection to be drawn; that brain
injuries can produce autistic spectrum disorder in those who did not have the condition
prior to their brain injury. The research into theory of mind has contributed greatly to an
understanding of these features.

Lewis rats: a model of autism. Behavioural Brain Research; Volume 100, Issues 1–2, 1 April
1999, Pages 43–50
39 Benson, DF & Miller, BL. Frontal Lobes: Clinical and Anatomic Aspects. . In Feinberg, T E &
Farah, M J. Behavioural Neurology and Neuropsychology. McGraw-Hill, New York, 1997.

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