1

Experience dependent maturation of emotional systems

of the brain in children with autism spectrum disorder (ASD)

2

Schore (2003) outlines a model of the experience-dependent maturation of the

brain’s evaluative system, also referred to as an appraisal system. The learning and

experience that lead to this maturation take place in large part within what Schore (2003),

and others, describe as a “resonant dyad” between a mother (or primary caregiver) and

infant. In this way, the social relationship created through the attachment bond between

mother and child becomes the primary environment for the self-organization of the

infant’s affect regulation and evaluative systems in the brain. However, in the case of

autism spectrum disorder (ASD), there is accumulating evidence that the important

precursors to the establishment of this resonant dyad are impaired or abnormal. In

particular, there appears to be abnormalities in the infant’s social attention mechanisms,

such as to faces and eyes, maternal tone of voice and other socially relevant stimuli. The

effect of these impairments would be to prevent the formation of the resonant dyadic

interaction in infancy, and consequently disrupt the experience-expectant development of

evaluative and emotional regulation systems in the brain (Nelson, 2000), in particular the

frontolimbic cortex (Schore, 2003). This hypothesis will be explored in light of current

behavioural and neuroanatomical findings in ASD. Implications of this hypothesis for an

intervention treatment for ASD will also be discussed.

The resonant dyad is created through the reciprocal social attention between the

caregiver and the child. From birth, a typically developing child will demonstrate

heightened “social attention” to faces, such as prolonged visual attention to face over

non-face stimuli (Johnson, Dziurawiec, Ellis, & Morton, 1991). A visual fixation

preference for face stimuli emerges around two months of age (Maurer & Barerra, 1981),

and infants will fixate on features within photographs of faces, giving particular attention

3

to the eye region (Maurer & Salpatek, 1967). A sample of five-month-olds demonstrated

sensitivity to small horizontal or vertical deviations in eye gaze (Symons, Hains, & Muir,

1998). This attention to the face, and the eye region in particular, leads to prolonged

periods of “intense mutual gaze” (Schore, 2003, p. 38) between mother and baby,

providing the primary forum for interpersonal communication. In typical development,

these prolonged periods of mutual gaze also provide the opportunity for “mirroring

sequences”, where mother and child simultaneously and instinctively match each other’s

facial expressions over short intervals of approximately 3 seconds (Beebe & Lachmann,

1988; as cited in Schore, 2003). Over the course of these sequences, the level of

engagement and positive affect between the dyad increases, peaks, and then returns to

equilibrium as first the infant and then the mother averts their gaze temporarily. When the

relationship is well attuned, the mother will wait for the infant’s signal to reengage in the

interaction again. In this way, the mother regulates the infant’s physiological arousal

from the intense emotional interchanges, and regulates information processing by

providing the stimulation in the appropriate doses and at the appropriate times (Schore,

2003). It is also hypothesized that through this process, the mother facilitates the infant’s

ability to tolerate increasingly higher levels of arousal, promoting development of the

infant’s emotion regulation system (Schore, 2003). Shared gaze is also important for the

development of social referencing and shared visual attention (Dawson, Meltzoff,

Osterling, Rinaldi, & Brown, 1998). At around 10-12 months of age, the infant begins to

socially reference his or her mother/caregiver when exploring their environment,

“reading” her emotional expression and following her gaze to objects (Schore, 2003). At

this stage in development, the child also begins to demonstrate pointing to communicate,

4

and joint attention; where the child will use shifts of gaze to look back and forth between

an object of interest and the caregiver, creating a “shared visual reality” (Schore, 2003).

This type of shared visual attention is thought to provide a foundation for later

development of theory of mind, as the child is able to understand that its own and

another’s perception of the world are distinct (and thus requires sharing).

Children with ASD, in contrast to this typical pattern, show abnormalities in

attention to faces. Decreased eye contact is known as one of the hallmark features of the

disorder. Evidence comes from a number of retrospective studies of home movies, which

show decreased levels of attention to faces compared to typically developing children

(e.g., Osterling, Dawson, & Munson, 2002) and at least one prospective case study

(Dawson, Osterling, Meltzoff, & Kuhl, 2000). Furthermore, a recent study of infants who

have an older sibling with a diagnosis of autism, and are therefore at higher genetic risk

for developing the disease, showed an abnormal pattern of visual attention to the mouth

instead of the eyes on a live video image of their mother during a facial interaction

paradigm (Merin, Young, Ozonoff, & Rogers, 2007). Therefore, infants with ASD have

far fewer opportunities for the intense mutual gaze interactions with their caregiver as

described above. They also do not go on to develop reliable pointing for the purposes of

sharing interest, or joint attention. In a study of gaze shifts between objects and people,

20-month-olds with ASD performed the majority of attentional shifts between two

objects, as opposed to between an object and a person, or two people. In contrast, the

typically developing and developmentally delayed control groups shifted attention more

frequently between an object and a person than between an object and another object or

between two people. The toddlers with ASD also spent less time in general looking at

5

people and looked for longer durations at objects, compared to the two control groups

(Swettenham et al., 1998).

Typically developing infants are also sensitive to the social signal of maternal

tone of voice. This type of vocalization often accompanies the mutual gaze interactions,

along with other gestures and body language (Schore, 2003). Sometimes referred to as

“motherese”, or “infant-directed”, this type of speech is characterized by higher pitch,

slower tempo, and exaggerated intonation contours (Grieser & Kuhl, 1988). Infants as

young as seven months not only discriminate between this infant-directed and normal,

adult-directed speech, but show a strong preference for the “motherese” (Pegg, Werker &

McLeod, 1992). Furthermore, study has shown that this type of speech is important for

language learning. When compared to adult-directed speech, motherese contains clearer

phonetic exemplars and may contribute to better phonetic discrimination in infants (Kuhl

et al., 1997). Additionally, the social responsiveness seen during these dyadic

interactions, where the mother responds with social reinforcement (e.g., smiling, moving

closer, touching) when the infant vocalizes, has also been shown to result in more mature

babbling in infants around 8 months of age. When mothers were socially responsive to

their infants within a short tests session (10 minutes), babbling was had more mature

voicing, syllable structure, and faster (canonical) consonant–vowel transitions, as

compared to infants who received the same number of social responses, but which were

not linked to their own production (Goldstein, King & West, 2003).

However, children with ASD do not show the typical preference for this type of

infant directed speech. One study used an electronic toy that played short recordings of

either the child’s mother’s voice or a blend of superimposed voices (similar to speech in a

6

crowded room) (Klin, 1991). Whereas typically developing children and developmentally

delayed children spent a significant majority of time listening to the mother’s voice, the

majority of the children in the ASD group spent more time listening to the superimposed

speech sounds (Klin, 1991). In a more recent study, “motherese” type speech samples

were contrasted with non-speech sounds, while matched on acoustic properties. The ASD

group showed a significant preference for the non-speech sounds, as compared to the

control group (Kuhl, Coffey-Corrina, Padden & Dawson, 2005).

Typically developing infants are also sensitive to other social stimuli, such as

responding to their name being called, or sounds produced by humans as opposed to

objects. Turning reliably to one’s name typically emerges around 5-7 months of age

(Dawson et al., 2004). When social sounds (e.g., calling infant’s name, humming a tune,

patting hands on thighs) were contrasted with nonsocial sounds (e.g., phone, whistle,

horn), children with ASD were reduced in orienting overall, but the impairment was more

pronounced for the social stimuli (Dawson et al., 2004).

The cause of these abnormalities is as yet unknown. One hypothesis is that

sharing attention with others, the downstream product of early social attention, requires

rapid shifting of attention back and forth between people and items of interest.

Courchesne, Chisum & Townsend (1995) suggest that difficulties with this rapid

switching may be the underlying cause. A second hypothesis suggests that inherent

complexity of social stimuli may be the issue, with an underlying problem in ASD being

difficulties with processing and representation of complex information (Dawson, 2004).

A third hypothesis is that the underlying deficit is in the reward system; such that social

stimuli are not appropriately tagged with rewarding value, and therefore do not attract

7

attention as they would for a typical child who finds social interactions inherently

rewarding (e.g., Dawson et al., 2005). But overall, a pattern of abnormal social attention

emerges in the children with ASD, which will consequently interfere with the typical

establishment of the resonant dyad between the infant and the primary caregiver. As a

result, the parts of the brain that require this type of input for typical maturation (i.e.,

experience expectant plasticity) will not develop typically. According to Schore (2003),

the intense visual and auditory stimulation that the infant receives during the face to face

interactions early in infancy are critical for promoting the growth of the prefrontal and

frontolimbic cortex, which are known to be important for emotion processing and

emotion regulation. One area of particular importance is the orbitofrontal cortex, (Schore,

1997, 2000, 2003). It is uniquely well positioned at the interface between cortical and

subcortical limbic structures, such as the insula, cingulate, and amygdala, but is also

afferently and efferently connected to autonomic structures, allowing it to both process

and regulate autonomic responses to environmental stimuli (Schore, 1997). According to

Schore (2003), during the process of the mother-child attachment interactions, the infant

is storing relations between the affective input from the mother’s face, voice, and body

language and its own internal emotional experiences. In this way, automatic appraisal

prototypes are formed and stored and form the basis of the infant’s own evaluative

system.

Consistent with this model, there is neuroanatomical evidence of abnormalities in

prefrontal cortex in individuals with autism spectrum disorders. One robust finding in

children with autism is significantly increased total brain volume. In a study by

Courchesne et al., (2001), 90 % of boys 2-4 years with ASD had larger than average

8

brain volumes, with an average of 18% more cerebral white matter, and 12% more

cerebral gray matter. Interestingly, these results seemed to follow a posterior to anterior

pattern, with frontal lobes most enlarged. Other studies of the white matter tracts in the

brain of individuals with ASD have also implicated the frontal cortex in particular. Using

diffusion tensor imaging (DTI), a measure of white matter tract integrity, results showed

reduced fractional anisotropy particularly in white matter adjacent to ventromedial

prefrontal cortex, anterior cingulate cortex, and the temporoparietal junction (Barnea-

Goraly, Kwon, Menon, Eliez, Lotspeich & Reiss, 2004). Frontal cortices have also been

implicated in studies of minicolumnar microstructure, where abnormally narrow

minicolumns were found in area 9 of the prefrontal cortex (Casanova, Buxhoeveden,

Switala, & Roy, 2002), and in a recent unpublished pilot study in the dorsal, mesial and

orbitofrontal areas of prefrontal cortex (reported in Courchesne & Pierce, 2005a).

Minicolumns in the cortex are thought to be the basic unit of information processing,

vertically integrated assemblies of pyramidal cells and interneurons which are arranged in

columns through the different lamina of cortex (Buxhoeveden & Casanova, 2002). These

minicolumns are thicker in association cortices, such as frontal areas, as compared to

primary sensory cortices. It is suggested that the thickness of minicolumns is proportional

to the amount of different information that is being integrated (Buxhoeveden &

Casanova, 2002).

Functional studies have also implicated abnormalities in frontal areas. An fMRI

study of the processing of socially familiar faces demonstrated a lack of activation in

medial frontal areas (including the anterior cingulate) in the ASD group, which was

significantly active in the typical control group (Pierce, Haist, Sedaghat, & Courchesne,

9

2004). Taken together, the evidence has led to the suggestion that the frontal cortices are

especially affected in autism (Courchesne & Pierce, 2005b).

Another area of the limbic system that is important for emotion processing and

regulation is the amygdala (LeDoux, 1996). Although Schore (2003) focuses on the role

of the orbitofrontal cortex in emotional “valence tagging”, the amygdala is thought to

play an important role in that function as well (LeDoux, 1996), and may be even more

important for associations that involve the more “basic” emotions such as fear, anger, joy,

sadness, disgust and surprise (Devinsky & D’Esposito, 2004). The amygdala has also

been shown to be abnormal in children with ASD (Acosta & Pearl, 2002). For example, a

recent study showed significantly larger volume of the left and right amygdala in children

with ASD as compared to typically developing children (Schumann et al., 2004).

However, other studies have been inconsistent, showing either enlarged or reduced

volumes of the amygdala (see Acosta & Pearl, 2002). The other important limbic

structure of the hippocampus has also been shown across studies to have abnormalities.

In particular, Kemper and Bauman (2002) found evidence of small, densely packed

neurons in amygdala, hippocampus, entorhinal cortex and mammilary bodies, upon

autopsy of nine children with autism compared to well matched controls. Thus it appears

that consistent abnormalities in well-known limbic structures, along with frontal

structures, are very commonly observed in neuroanatomical structures of ASD.

However, it is important to note that in the case of autism, that the relationship

between neural abnormalities and lack of attachment-based experiential input is likely not

unidirectional. It is more probable that the relationship for this disorder is bidirectional.

That is, certain genetically based neural abnormalities precede, and lead to, the

10

abnormalities in social orienting detailed above. However, the lack of environmental

experience normally gained from the attachment relationship is a critical factor for further

experience-dependent maturation of emotion systems within the brain. More specifically,

without the typical development of the social attachment relationship, the brain will be

left to self-organize in a relatively non-social environment. This is consistent with

common behavioural observations of children with ASD as they grow up, such as a lack

of interest in others, solitary, repetitive play, interest in objects or parts of objects.

Evidence for this comes from behavioural observations, such as the home movies

mentioned earlier, and studies such as the one conducted by Swettenham and colleagues

(1998), showing that children with ASD spent more time looking at objects that people,

and frequently looked from object to object, but very infrequently back at a person.

Objects and solitary repetitive activities become attractor states that reinforce the

withdrawal from the social world, leading to further deprivation of social interactional

experience. This will also lead to further deficits in learning in general, as studies have

also begun to show the importance of social contexts for learning, such as language

acquisition. In a study by Kuhl, Tsao, and Liu (2003), two groups of infants received

identical exposure to a second language for a brief but intensive time period. However,

one group of infants was exposed to the second language in a live social context, with an

examiner reading a story. The second group was exposed in a non-social context, using

audio-visual presentation of the same examiner reading the story. Results showed that

infants who were exposed to the language in the live, social context showed preserved

phonetic discrimination for the second language; whereas infants who were exposed to

the non-social condition could not discriminate the phonemes (Kuhl et al., 2003). Thus,

11

mere exposure to the second language was not sufficient; the exposure had to take place

in a social context. This finding is consistent with Schore’s (2002) notion of learning and

development taking place within a social relationship. As the infants grow and develop,

relationships expand out from the primary caregiver to include other members of the

family, friends, teachers, and other members of the community. However, as the neural

systems in a child with ASD continue to self-organize within non-social contexts, this

becomes more and more difficult for them to achieve. Furthermore, deficits in the neural

development of the emotional regulation system, due to deprivation of normal social

experience, will lead to difficulties regulating emotion or dealing with distress. This will

lead to abnormal coping and soothing strategies, which often focus around objects and

repetitive sensory stimulation.

More recent types of behavioural interventions for children with ASD are also

consistent with this hypothesis. One method of therapy, known as the developmental,

individual-differences, relationship-based (DIR) model, otherwise known as floortime,

reflects this goal of establishing a social relationship with the child to promote learning.

The overall goals of the floortime technique are to follow the child’s lead, and through

the therapist or family members actions and emotional expression, to “woo the child into

engaging”. The goal is to intrude on the child’s play in a way that forces them him or her

to engage socially in order to achieve their goals, and gradually increase the social

demands of the interaction over time, being sensitive to the child’s developmental level

and particular sensitivities or challenges. Interestingly, aspects of the technique as

described by a senior clinician using the model are similar to Schore’s (2003) description

of the resonant dyad. For example, following the child’s lead, creation of circles of

12

communication that open, build, and close (Greenspan, 2000; as cited in Hess, 2004).

However, the technique also requires intrusion and intentional shaping of the child’s

behaviour, as opposed to the completely natural and instinctive interactions with a

typically developing infant. The approach has been criticized because as yet there have

not been any systematic, randomized, controlled studies of outcome. However, the

technique has won support with parents and professionals who have anecdotal evidence

of its positive effects. Although further study is required before the mechanisms

underlying success of the floortime technique will be elucidated, based on Schore’s

description we can infer that this type of therapy attempts to create a social relationship

within which learning can occur. It is possible that for some children with ASD, this type

of intervention is able to establish a resonant dyad. The duration of this dyadic interaction

starts off extremely brief, but if successful can increase in duration and eventually have

impact on the child’s engagement and response to the social world. Presumably this is

happening at a neural level and may be able to reverse some of the abnormal

development that has occurred. Studies of neural structure and function before and after

this type of intervention would be extremely interesting and beneficial.

Children with an autism spectrum disorder exhibit abnormal social orienting in a

number of different domains early on in life. These deficits, likely attributable to

genetically based neural abnormalities, result in difficulty establishing a resonant dyadic

relationship between the infant and caregiver, and it is hypothesized that this lack of

social experience in turn results in further abnormal neural development in the areas of

the brain involved in emotion regulation and appraisal; namely the prefrontal cortex and

limbic system. Consistent with this hypothesis, these areas are the major areas where

13

structural abnormalities have been observed in ASD. Without intervention, the infant’s

brain will continue on a self-organizing trajectory in a relatively nonsocial world, as

compared to a typically developing child. This hypothesis is consistent with some

observed symptoms in autism, such as social avoidance and focus on objects and solitary

repetitive behaviours. Furthermore, the lack of social contexts may put children at a

disadavantage for learning in general, such as in the domain of language acquisition.

However, interventions are being explored which contain elements of the dyadic social

relationship described by Schore (2003). These interventions may be able to slow or

reverse the abnormal neural development in children with ASD, and provide mechanisms

for creation of social contexts to promote learning. Further research is needed to explore

the outcomes and mechanisms of these types of interventions.

Comments:

Nice job! The stylish and polished quality of your writing and argumentation

is excellent. You are very clear, the writing is almost transparent in its clarity, and

you integrate your claims with evidence smoothly and seamlessly throughout. Your

discussion of neural systems and their interrelations is generally spot-on. Excellent

precision in your individual points and good development of your arguments from

point to point.

I’m glad you recognized the potential confounds and circularity of proposing

the dyadic relationship as a causal factor. You dealt with this problem quite well,

and the image of an ongoing self-organizing trajectory, free of the parental

constraint, was quite persuasive and effective. Still, I think this was where you could

14

have built a stronger essay. You could have differentiated, based on what you know

of the brain and development, between the kind of anomalies likely to lead to the

breakdown of dyadic resonance and the kind likely to follow. This watershed notion

should be really strong, should even be the backbone of the model. Otherwise, it

seems a bit arbitrary that the attachment relationship suddenly steps up to the plate

(of causation) at some point along the way. Also, to say that the interaction between

the neural anomalies and the breakdown of the dyad is bidirectional is a critical

point. Again, good that you made it, but better to make more of it. Bidirectional

causation of this sort has all kinds of cool qualities—such as the likelihood of

positive feedback, phase transitions (sudden switches) in the trajectory over time,

etc. In fact, S-O can only result in systems where there is bidirectional causation (viz

positive feedback). Finally, since you make Schore’s model so central, why not argue

that the OFC is specially poised to be an effect rather than a cause in the ongoing

trajectory. This would be most powerful. I got a great paper from a student a few

years ago, arguing that lower brain anomalies (brainstem issues, and maybe those

amygdala differences you mention) are prespecified neural anomalies, but cortical

differences then manifest themselves, as a developmental cascade, completing the

picture of how autistic brains differ. I think that kind of argument is most powerful,

and you could link it with the role of the attachment relationship to make a very

tight case.

Paper: A/A+

15

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