Neuropsychological studies of Autism Spectrum Disorders Notes for a talk given on 27th September, Kanazawa By Uta Frith
When Leo Kanner, the Baltimore Child Psychiatrist, first described the condition he called ‘infantile autism’, he identified 3 core features: Inability to relate affectively to others Insistence on sameness Islets of ability
Autism has a short history but there have been major advances. Only 70 years ago were there was barely a recognition of autism, although already some very first descriptions appeared. Now we know that there is a whole spectrum of autistic disorder, from mild to severe. We know it is a life-long disorder with a basis in the brain. So we are in a position to describe the nature of autism and begin to ask about the genetic causes of the condition.
While only 50 years ago there was much speculation about a psychogenic cause of autism, now everyone agrees that there is a biological basis of autism and that there is brain abnormality. But, we do not yet have biological markers. We define autism spectrum disorders in terms of behavioural criteria.
Everyone agrees on three key behavioural criteria, already identified by Kanner, But not everyone agrees on how to explain the behavioural signs. We need to consider explanations of behaviour at the cognitive level and at the brain level.
No single cognitive theory is sufficient to explain the core behavioural features of autism. At present we have three theories which are needed to explain the social problems, the everyday coping problems, and the cognitive strengths (islets of ability). The three theories are: “Mindblindness”, “Executive Dysfunction”, “Weak Central Coherence”.
I start with the “Mindlblindness Theory”. This theory explains many of the behavioural signs of autism in social interaction and communication. These signs are present from the second year of life and remain lifelong. They change in their behavioural manifestation over the course of development. Their different forms can be explained quite well by mindblindness, or poor mentalizing ability. Mentalising refers to our pervasive and automatic ability to attribute mental states to others, that is, to read other minds.
This test, known as the Sally-Anne test, is a way of explaining what is meant by mentalising ability is. The test can be enacted with dolls or with real people. This makes no difference. This test was first published in 1985 (Baron-Cphen, Leslie & Frith) and these are the dolls that were used then. ”Here is Sally and here is Anne. Sally has a basket and Anne has a box. Sally has a marble. She puts it in her basket. She covers the basket with the cloth.”
“Sally goes out to play. While Sally is out, Anne, naughty Anne, takes the marble out of Sally’s basket and puts it into her own box.”
“Now Sally comes back and wants to play with her marble. Where will Sally look for the marble?” The correct answer is “in the basket”, because this is where Sally thinks the marble is. She could not know that Anne transferred the marble to the box, because she was not in the room at the time the transfer happened. Therefore Sally now has a false belief: she believes the marble is in the basket. Her belief explains what she will do next. The reality, where the marble actually is, does not explain what she will do next. A belief is a typical mental state. We use mental states, rather than reality, to explain what people are going to do. This is what we mean by mentalising, or mindreading. Five-year old normally developing children understand this perfectly, but not autistic children. Autistic children say that Sally will look for the marble where it really is (in the box).
&lt;number&gt; Many experiments have investigated mentalising ability, e.g. the attribution of a false belief to another person, in autistic individuals. These experiments have shown that autistic children can over many years learn to mentalise after a fashion. This never becomes spontaneous or automatic. Autistic adults with normal or high intelligence (on the mild end of the spectrum of autistic disorders) can pass the Sally-Anne test with ease. Still they have problems in real life. For example they have difficulty in attributing mental states spontaneously to animated shapes in silent movies. Heider and Simmel in 1945 have shown that normal adults attribute mental states to animated shapes automatically. This is known as the Heider & Simmel effect. So, we are compelled to perceive a (carefully scripted) sequence of moving triangles as interacting with each other. This can be contrasted with randomly moving triangles. In this case we are not tempted to attribute mental states to them, but we perceive them as moving randomly.
&lt;number&gt; It is possible to use functional Magnetic Resonance Imaging (fMRI) to reveal the brain’s mentalising system. This is done by contrasting two condition. In one condition, the person in the scanner watches interacting triangles. In the other condition the person watches randomly moving triangles. The comparison shows the extra activity in the areas of the brain when we see interacting triangles and spontaneously mentalise. This is known as the subtraction method of neuroimaging. It shows us where in the brain the activity occurs that is of interest to the experimenter.
Here is an example of a carefully scripted sequence of triangles interacting with each other. We spontaneously attribute mental states to them (we mentalise). For example, here we see a scenario where the big triangle tries to get the little triangle to come outside to play. The little triangle seems to be afraid to go outside, but eventually is persuaded by the big triangle to go outside and play. Normal adults often perceive the meaning of the sequence as a mother trying to gently coax the child to go outside the house. People with autism find it very difficult to get this sort of meaning.
&lt;number&gt; Here is an example of a sequence of randomly floating triangles. This movie does not invite mentalising. The triangles are not perceived as interacting. People with autistic spectrum disorder have no difficulty in seeing randomly floating triangles.
&lt;number&gt; This slide shows where the extra brain activity occurs when we subtract brain activation found while watching interacting triangles from brain activation found while watching randomly moving triangles. This subtraction method reveals a brain system involving three main components shown on the slide: Medial prefrontal cortex, Superior temporal sulcus and periamygdaloid region. This is now known as the brain’s mentalising system. This system has been revealed in a number of different neuroimaging studies with different stimuli, for example, short stories, which in one condition do involve mentalising and in another condition do not involve mentalising. The components of this brain system are working in concert in normal people and are all highly active during mentalising.
&lt;number&gt; In autism the mentalising system shows reduced activation and there is weak connectivity between its components.
This slide shows activation in the mentalising system in both normal adults (light blue) and adults at the mild end of the autism spectrum (dark blue), while watching the interacting triangles across a number of different animations. In autistic adults activation is reduced in the main components of the mentalising system: the 3 columns on the right of the figure. In the visual processing areas of the brain (the leftmost column) activation was equally high in normal and autistic individuals. This shows that autistic people can visually distinguish the two types of animations very well and the visual regions respond with greater activity to the interacting triangles. However, autistic people cannot interpret the meaning of these visually very different animations.This interpretation depends on top-down input from the main components of the mentalising system. In the case of autism the connectivity between the visual regions the mentalising regions is weak.
&lt;number&gt; Most studies on mentalising in autism concern reading other minds. What about reading own mind? We know from autobiographies that people with autism have difficulties describing their own inner mental states, and in particular their own feelings. Why is this? Do they not have the feelings? Are they not aware of the feelings? Or, are they not aware of having the feelings?
&lt;number&gt; We conducted an fMRI experiment where people with mild autism spectrum disorder and normal adults were asked to introspect on their own feelings while watching pictures. These pictures were taken from the International Affective Picture Scales. Some pictures arouse pleasant feelings, others unpleasant feelings. Our subjects were asked to indicate on a sliding scale how each picture made them feel. They were then shown the same pictures again. But this time they had to indicate, again on a sliding scale, how much colour was contained in each picture. This enabled us to find out the extra activity in the brain when people introspected on their inner feelings, and when they just evaluated the colour content of the stimuli. We could also compare brain activity when pleasant and unpleasant pictures were shown, regardless of the task.
&lt;number&gt; Here are the different comparisons of brain activation that we made in this study. We compared what happened when people evaluated their inner feelings vs evaluating colour. Here the mentalising system was active. This system is involved in reading minds. Not only other minds, but also own minds. 2. We compared what happened when people evaluated their inner feelings in the presence of unpleasant vs pleasant picture. Here the Anterior Insula was active. This region is known to be active when people feel pain and bodily sensations. 2. We compared what happened when people were simply exposed to unpleasant vs pleasant pictures. This activated the Amygdala system of the brain. This is known to be active when people are aroused by strong negative emotions.
&lt;number&gt; This slide shows the extra brain activation in the mentalising system of the brain (medial prefrontal cortex, superior temporal sulcus) when people introspected on their own feelings vs evaluating the colour content of the picture. In the circled areas there was a significant group difference: People with autism showed reduced activation in these regions compared to normal adults.
&lt;number&gt; This slide shows in a schematic way how we might answer the three questions posed at the beginning of this study. Do autistic people not have feelings? No. Autistic people do have feelings. Their amygdala system was just as active as that of normal people when exposed to unpleasant pictures. 2. Are they not aware of the feelings? Yes and no. Autistic people are aware of the feelings to the extent that they are able to identify their own feelings. This shows individual differences. About half the people in the autism group were not good at identifying their own feelings. These people showed less activation in the Anterior Insula than the others in the group. Are they not aware of having the feelings? Yes. Autistic people are not aware of themselves as having feelings - at least not to the same extent as normal people. They cannot read their own minds. My interpretation is that perhaps there is no inner ‘self’ to read the feelings, as represented by the amygdala and anterior insula systems. Autism could mean an ‘absent self’.
Autism is not only characterised by difficulties in social interaction and communication. There are non-social difficulties as well. The theory of executive dysfunction tries to explain these difficulties. Executive function is an umbrella term for a range of higher-order control processes which are needed to act flexibly in novel or complex situations. Poor executive control is associated with poor frontal lobe function. By analogy, autistic people suffer from poor frontal lobe function.
This slide shows two popular neuropsychological tests, Wisconsin Card Sorting and Tower of London. Autistic people tend to perform poorly on these tests. They tend to perseverate on sorting when dimensions on the Wisconsin test are switched by the experimenter, and they tend to make poor plans on the Tower of London test.
Laboratory tests of executive functions confirm the nature of the difficulties that autistic people experience in their everyday life. Examples are: Not being able to inhibit no-longer-useful behaviour (perseveration) Not being able to respond flexibly in the face of change Not being able to plan ahead Not being able to monitor behaviour to check when goal is reached Not being able to hold in mind several things at once All these difficulties are apparent when autistic people have to do their daily shopping in a supermarket, for example.
The same advice that is used to rehabilitate patients with frontal lobe damage is also useful for autistic people. Most intervention programmes for autism are geared to alleviate executive function problems. Typically these programmes involve the following points: Give clear structure Give constant prompts and reminders Give outside support There are techniques for routinising behaviour, for coping with novelty and for coping with anxiety. These all benefit autistic people, even those at the mild end of the autism spectrum.
A deficit account, such as the executive dysfunction account, cannot explain the cognitive strengths and islets of ability in autism. One theory that tries to explain these strengths (fascination with small details, superior perceptual discrimination, savant skills) is: Weak Central Coherence.
Weak Central Coherence is an information processing style: a tendency to process details at the expense of global meaning This is the opposite to strong central coherence where global precedes local. Weak Central Coherence as a processing style is found also in relatives of individuals with autism, who are themselves not at all autistic. This style has advantages when analytic skills are required, but can have disadvantages when overall meaning is crucial
The Embedded Figures Test is performed well by people with a Weak Central Coherence processing style. They find the small detail in the overall pattern very easily and quickly.
These examples show tests where autistic individuals often show superior performance compared to IQ- matched controls. (A) Block Design subtest of the Wechsler intelligence test is often a cognitive strength in the profile of performance. (B) locating embedded figures is often a cognitive strength. (C) copying of impossible figures has been shown to be superior. (D) Ebbinghaus illusion: the surrounding elements can make the (identical) central targets appear quite different. Autistic observers are less susceptible to this illusion. However there is some controversy about this finding. (E and F) Autistic observers are faster and less error prone at finding the odd-man-out in cluttered displays whether the target is defined by a single feature as in (E) or by a conjunction of features as in (F). (G) Observers with ASD can tolerate higher levels of noise in determining the orientation of luminance-defined sine-wave gratings (Bertone et al. 2005).
An example of the bad effect of exreme Weak Central Coherence is from the movie Rainman. Rainman walks across the street. Suddenly the traffic lights change to red. He immediately stands still in the middle of the traffic, a very dangerous situation. Rainman interprets the red signal without concern for the overall meaning. Having already started to cross the road, he should not stop at the red signal. Instead Rainmain should hurry up to get across, or go back. This example also shows that Weak Central Coherence can be understood as a kind of Context-blindness. This is a disadvantage of this processing style. In the extreme case the result is a fragmentary world.
We can now ask the question whether there is a common explanation for both the social and non-social features of autism. One common denominator is that autistic people do not live in a shared social world or shared physical world. What is the reason for this? Perhaps the cognitive system lacks some innate basic preferences. Perhaps information is processed without being guided by prior expectations. Perhaps perception does not use prediction. This hypothesis brings together the idea of an absent self and the idea that context has little effect on perception. The hypothesis suggests a lack of top-down modulation.
This is an example to explain what I mean by top-down modulation. The first slide gives a picture that seems completely chaotic, without meaning. There is no prior expectation to guide our perception. Anybody who has not seen the following slide should say that they have no idea what this is a picture of. But, once you have seen the second slide, you will know what it is.
Here we get an expectation of what it is that the first picture shows. It is a cow. We now can use this information (top-down modulation) to look again at the first picture.
Top-down modulation has transformed our perception. Now it is completely clear what this picture is. A cow. We see better when we have an expectation of what to see. Is autistic perception always like our perception was when we saw the first picture? Due to a lack of top-down modulation?
What is meant by top-down modulation? The opposite of Top-down is Bottom-up. Here the idea is proposed that there are two kinds of neurons: driving neurons (= bottom up) and controlling neurons (= top-down). The proposal is that in the autistic brain these two neural systems don’t connect well together.
What happens in the brain during top-down modulation? A brain imaging experiment gives some clues. This experiment was first conducted by Vuilleumier (2001). Bird et al. repeated this experiment with autistic adults. Again these individuals were at the mild end of the autism spectrum.
This slide shows the design of Vuilleumier’s fMRI experiment (2001), which was also used by Bird et al, 2003. People in the scanner are told in advance whether to attend to the horizontal or vertical location where pairs of faces and pairs of houses are shown for a split second. They have to say whether a pair is the same or different. The brain activation in the region that processes faces is enhanced, when faces are shown in the attended location. Vice versa, brain activation in the region that processes houses is enhanced when houses are shown in the attended location. This is an example of top-down modulation.
The results of Bird et al.’s experiment were clear: autistic people showed much less enhanced activation in either the face or the house processing regions of the brain. This is evidence for a lack of top-down modulation. This lack of top-down modulation is particularly striking in the case of faces. This is interesting as people with autism often seem to find faces difficult to identify.
In the fMRI experiment too there was evidence for a lack of top-down modulation. In the slide earlier on, we saw that the visual areas of the brain were activated in a normal way, but the components of the mentalising system which are more anterior in the brain, did not show increased activation in autism. Autistic people can distinguish visually the interacting and randomly moving stimuli, but they can’t interpret them.
There is an interesting speculation (due to Chris Frith, 2003) about the reason that top-down neurons are not efficient and not well-connected with driving neurons in the autistic brain. The idea is that brain reorganisation early in development is faulty. Perhaps it is precisely the controlling, neurons which are not reorganised as they proliferate in development during the first two years of life. It has been suggested that there is a failure of pruning in the young autistic brain, resulting in bigger brains. This failure could be specific to controlling neurpns. Driving neurons, on the other hand, may not be so affected. Perhaps they need less reorganisation, as they are functioning already from birth. This combination could explain the superior perception of detail (efficient driving neurons) with an apparent inability to take into account higher level context and prior expectations (inefficient controlling neurons).
The speculation about brain re-organisation in early life is only speculation. It still needs to be tested. This could be done by longitudinal studies and using high-field scanners. This is an exciting programme of research for the future.
I am tempted to provide even more speculation: inefficient controlling neurons may lead not only to poor top-down control, but may also result in a poor idea of the self. The ‘absent self’ would explain why there are executive function problems, and why there are problems in reading own and other minds. There is no self to do the mind-reading. I use the analogy for the self as the chief executive of a big company. The staff of the company are working well by themselves and the chief executive only needs to intervene in certain situations, when problems arise and when priorities have to be set. This can be a strength: basic level sensory processes may flourish and may dominate behaviour. But this can also be a weakness: Basic level processes may overwhelm perception. We know from the study I presented earlier that autistic people have strong feelings, but do not realise that it is themselves who have the feelings. Thus the autistic individual may suffer the fate of a feather in the storm of sensations.
Acknowledgements to my friends and colleagues and to the MRC for funding this research.
U.Frith Neuropsychology of autism. Talk given at Kanazawa+notes 2007
Neuropsychological studies of
Autism Spectrum Disorders
31st Annual Meeting of the Neuropsychology
Association of Japan
27th September Kanazawa
Infantile Autism Kanner 1943
Inability to relate affectively to others
Insistence on sameness
Islets of ability
2 Uta Frith Kanazawa September 2007
A little bit of history
100 years ago
autism not recognised at all
70 years ago
autistic children first described in the Netherlands, in the US,
50 years ago
psychosocial origin presumed - not brain abnormality
progress towards identifying brain abnormality, genetic risk
factors and other putative causes
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Everyone agrees on
a biological basis for autism
Autism is a biologically based condition
With a strong genetic component
With its effect on brain development
There is some brain abnormality
We do not yet have biological markers
4 Uta Frith Kanazawa September 2007
Everyone agrees on
three key behavioural signs
Difficulties in Social interaction
Difficulties in Communication
Restricted Patterns of Behaviour
Not everyone agrees on how to explain these
- at the cognitive level - at the brain level
There are different cognitive theories
These have led to new knowledge
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No single theory is sufficient
Three cognitive theories are needed
- at least -
To explain social and communication problems
– E.g. Mind blindness
To explain everyday coping problems
– E.g. Executive dysfunction
To explain cognitive strengths
– E.g. Weak central coherence
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Deficits in Social Cognition are a Core
Feature of Autism
One hypothesis explains many of the problems in
communication and social interaction that are
obvious from the second year of life
Poor mentalizing ability
A missing capacity due to specific brain abnormality
• Affecting the intuitive ability to “read minds”
• Leaving intact other social capacities
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Baron-Cohen, Leslie and Frith, 1985: Sally-Anne test
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Sally (mistakenly) thinks her marble is in the basket
Autistic children typically fail this test
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Able autistic people can learn to read
other minds but subtle problems persist
Klin, 2000; Abell et al. 2000; Castelli et al. 2002
Example: Heider & Simmer effect
We are often compelled to attribute mental states to
Two triangles interacting together
Two triangles just floating
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Revealing components of the brain’s
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Comparison shows extra activity
when we see interactions and mentalise
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are needed to see this picture.
13 Uta FCritho mKaena ozauwt aa Snedp tepmlabye r- 2 i0t0’s7 nice out here.
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are needed to see this picture.
14 Uta Frith Kanazawa September Animation that does not invite me2n00ta7 lising drifting…floating…
Superior temporal sulcus
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Castelli et al., 2000
Basal temporal, periamygdaloid
Mentalising system in the autistic brain
Weak connectivity between components
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Brain activity associated with mentalizing in normal and autistic Ss
R. extra-striate R. basal temporal R. STS R. medial prefrontal
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V3 LO temporal
Castelli et al 2002
In autism reduced connectivity between V3 and anterior regions
What about reading own mind?
Many people with autism say
• they cannot describe their own feelings
• Do they not have the feelings?
• Are they not aware of the feelings?
• Are they not aware of having feelings?
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Monitoring own feelings
How does the picture make you feel?
Pleasant - Neutral - Very unpleasant
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QuickTime™ and a
TIFF (Uncompressed) decompressor
are needed to see this picture.
Being aware of having the feelings
Monitoring inner feeling compared to picture colour
Mentalizing system active
Being aware of the feelings
Introspecting on feeling evoked by unpleasant picture compared to
feeling evoked by nice picture
Anterior Insula active
Actually having the feelings
Looking at unpleasant picture compared to nice picture
Amygdala - orbitofrontal system active
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Monitoring feelings - Mentalizing system active
Reduced activation in autism
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22 Uta Frith Kanazawa September 2007
Aware of having feelings
Aware of feeling
The non-social difficulties
• A range of higher-order control processes
• Needed to act flexibly in novel or complex situations
Poor executive control is associated with poor frontal
lobe function and explains a range of problem
behaviours in people with ASD
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Examples of executive function tests
performed poorly by people with ASD
Wisconsin Card sorting Tower of London
Think about different dimensions for sorting
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Plan several steps ahead
Don’t forget the rules
What symptoms can be explained by
executive function failure?
Not being able to
• inhibit no-longer-useful behaviour (perseveration)
• respond flexibly in the face of change
• plan ahead
• monitor behaviour to check when goal is reached
• hold in mind several things at once
25 Uta Frith Kanazawa September 2007
How to cope with
poor executive control?
• Give clear structure
• Give constant prompts and reminders
• Give outside support
• Specific techniques
– For routinising behaviour
– For coping with novelty
• Coping with anxiety
Most intervention programmes are geared to
alleviate executive function problems
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also need to be explained
Weak central coherence Theory (WCC)
attempts to explain
• Fascination with small details
• Superior perceptual discrimination
• Savant skills
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Explaining the non-social features
Weak central coherence
• WCC an information processing style
– tendency to process details at the expense of global meaning
– opposite to strong central coherence where global precedes local
• More likely in relatives of individuals with autism
• Advantages when analytic skills are required
• Disadvantages when overall meaning is crucial
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Embedded Figures Test
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Cognitive strengths in autism
(A) Block Design subtest of the Wechsler intelligence test, (B) locating embedded figures, (C)
copying impossible figures. (D) identifying target size in Ebbinghaus illusion.
(E and F) Finding the odd-man-out in cluttered displays whether the target is defined by a single
feature as in (E) or by a conjunction of features as in (F).
(G) tolerating higher levels of noise in determining the orientation of luminance-defined sine-wave
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Weak central coherence
can produce problems in everyday life
A fragmentary world
• Inability to use context to make sense
• Diminished top-down influences on
Example: walk - don’t walk
different actions can be required even with identical
signal depending on context
31 Uta Frith Kanazawa September 2007
QuickTime™ and a
TIFF (Uncompressed) decompressor
are needed to see this picture.
A common denominator for social and
non-social symptoms of ASD?
• No shared social world
• No shared physical world
• The cognitive system lacks some basic preferences
• Information is processed without prior expectations
– As if anything is possible
• Perception does not use prediction
no TOP and no TOP-DOWN MODULATION
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What is this?
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The same picture again: Obviously it is a cow !
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Bottom-up vs Top-down in the Brain
Two kinds of neural systems
driving neurons: bottom-up input
controlling neurons: top-down expectations
The two systems don’t connect well together
Hence poor top-down modulation
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TIFF (UQnucicokmTpimrees™sed a)n dde caompressor are needed to see this picture.
What is meant by TOP-DOWN?
What happens in the brain during top-down modulation?
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“Attend to vertical (horizontal) location”
Geoff Bird, Caroline Catmur,
Giorgia Silani, Uta Frith and
Chris Frith (2003)
Before picture flashes up
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When expecting to
see faces or houses
in one of two
activity in the is
enhanced in the
brain regions that
process faces or
Fusiform Face area
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(a) Attentional modulation of response
in fusiform gyrus at x = - 42, y = - 80, z = - 12
% Signal Change
(b) Attentional modulation of response
in parahippocampal gyrus at x = - 26, y = - 46, z = - 12
% Signal Change
Evidence for lack of top-down
The difference in the response when
attended and unattended
Less modulation in Fusiform Face Area
in Parahippocampal Place Area
Evidence for lack of top-down modulation
• Visual areas detect mentalizing stimuli and
process them in detail
• but higher-level processes fail to interpret them
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A speculation about brain reorganisation
Cognitive deficits may reflect disconnections
between driving and controlling neurons
Disconnections may be a consequence of lack of
appropriate pruning of re-entrant (backward)
connections during the early years of life
(Chris Frith, 2003)
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Causes of TOPMOD failure
• Brain re-organisation may fail in first two years of life
– Probably under genetic control
• To test this we would need to study actual progress of
brain reorganization in development
• Ideally using longitudinal high-field scanning
An exciting programme for the future
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Even more speculation… “The absent self”
• High-order control system in the brain = self
• Provocative idea: In autism - this self is absent or weak
• The individual lacks awareness of this self and cannot
reflect on own feelings
• Analogy of absent chief executive of a big organisation
– staff are working well and problems arise only in certain situations,
e.g. when priorities have to be set.
• Can be strength: basic level sensory processes may
flourish and may dominate behaviour
• Can be weakness: Basic level processes may overwhelm
• Thus individual may suffer the fate of a feather in the storm
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Thanks to my colleagues and collaborators
Francesca Happé, Chris Frith,
Fulvia Castelli, Elisabeth Hill, Geoff Bird, Rachel
Brindley, Giorgia Silani, Tania Singer
and Sarah White
Thanks to the MRC for funding this research
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