Article

Kennedy DP, Courchesne EFunctional abnormalities of the default network during self- and other-reflection in autism. Soc Cogn Affect Neurosci 3:177-190

Department of Neurosciences, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0662, USA.
Social Cognitive and Affective Neuroscience (Impact Factor: 7.37). 07/2008; 3(2):177-90. DOI: 10.1093/scan/nsn011
Source: PubMed
ABSTRACT
Recent studies of autism have identified functional abnormalities of the default network during a passive resting state. Since the default network is also typically engaged during social, emotional and introspective processing, dysfunction of this network may underlie some of the difficulties individuals with autism exhibit in these broad domains. In the present experiment, we attempted to further delineate the nature of default network abnormality in autism using experimentally constrained social and introspective tasks. Thirteen autism and 12 control participants were scanned while making true/false judgments for various statements about themselves (SELF condition) or a close other person (OTHER), and pertaining to either psychological personality traits (INTERNAL) or observable characteristics and behaviors (EXTERNAL). In the ventral medial prefrontal cortex/ventral anterior cingulate cortex, activity was reduced in the autism group across all judgment conditions and also during a resting condition, suggestive of task-independent dysfunction of this region. In other default network regions, overall levels of activity were not different between groups. Furthermore, in several of these regions, we found group by condition interactions only for INTERNAL/EXTERNAL judgments, and not SELF/OTHER judgments, suggestive of task-specific dysfunction. Overall, these results provide a more detailed view of default network functionality and abnormality in autism.

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Available from: ncbi.nlm.nih.gov
Functional abnormalities of the default network
during self- and other-reflection in autism
Daniel P. Kennedy,
1
and Eric Courchesne
1,2
1
Department of Neurosciences, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0662, and
2
Center for Autism
Research, Rady Children’s Hospital Research Center, 8110 La Jolla Shores Drive, Suite 201, La Jolla, CA 92037, USA
Recent studies of autism have identified functional abnormalities of the default network during a passive resting state. Since the
default network is also typically engaged during social, emotional and introspective processing, dysfunction of this network may
underlie some of the difficulties individuals with autism exhibit in these broad domains. In the present experiment, we attempted
to further delineate the nature of default network abnormality in autism using experimentally constrained social and introspective
tasks. Thirteen autism and 12 control participants were scanned while making true/false judgments for various statements about
themselves (SELF condition) or a close other person (OTHER), and pertaining to either psychological personality traits (INTERNAL)
or observable characteristics and behaviors (EXTERNAL). In the ventral medial prefrontal cortex/ventral anterior cingulate cortex,
activity was reduced in the autism group across all judgment conditions and also during a resting condition, suggestive of task-
independent dysfunction of this region. In other default network regions, overall levels of activity were not different between
groups. Furthermore, in several of these regions, we found group by condition interactions only for INTERNAL/EXTERNAL
judgments, and not SELF/OTHER judgments, suggestive of task-specific dysfunction. Overall, these results provide a more
detailed view of default network functionality and abnormality in autism.
Keywords: autism spectrum disorders; retrosplenial cortex; posterior cingulate cortex; default mode; rest
INTRODUCTION
Several recent studies of autism have identified functional
abnormalities of the default network (Kennedy et al., 2006;
Cherkassky et al., 2006; Kennedy and Courchesne, 2008).
This network, comprised of the medial prefrontal cortex
(MPFC)/ventral anterior cingulate cortex (vACC), retro-
splenial cortex/posterior cingulate cortex (RSC/PCC) and
angular gyrus (ANG), among other regions, is so named
because it exhibits high levels of metabolic activity at rest, in
the absence of an externally imposed cognitively demanding
task (Raichle et al., 2001). In other words, the brain defaults
to this pattern of activity when allowed to rest. Interestingly,
similarly high activity of this network is also seen when
typical subjects engage in tasks of a social, emotional or
introspective nature (Fletcher et al., 1995; Maddock, 1999;
Gusnard et al., 2001; Maddock et al., 2001; Iacoboni et al.,
2004; Ochsner et al., 2004, 2005; D’Argembeau et al., 2005;
Cavanna and Trimble, 2006; Northoff et al., 2006)the very
tasks which are most difficult for individuals with autism
(Kanner, 1943; Hurlburt et al., 1994).
Along with the few studies that have explicitly examined
resting functionality or resting functional connectivity of the
default network in autism (Kennedy et al., 2006; Cherkassky
et al., 2006; Kennedy and Courchesne, 2008), other studies
have also found abnormalities in regions of the default
network (and, in particular, the MPFC) during a variety of
socioemotional tasks. For instance, such abnormalities have
been noted during viewing of personally familiar faces
(Pierce et al., 2004), reading of negatively valenced
emotional words (Kennedy et al., 2006) and in a mentalizing
task, where subjects observed geometric objects moving in
particular ways to imply intentionality (Castelli et al., 2002).
Importantly, there are at least two different explanations
for the pervasiveness of functional abnormality in default
network regions across both socioemotional tasks and no-task
resting conditions. First, perhaps regions of this network are
simply unable to function properly in individuals with
autism, regardless of the task being performedin other
words, a task-independent dysfunction. Alternatively, how-
ever, such abnormalities may simply reflect the known
impairments of individuals with autism to automatically
engage in socioemotional and introspective processes, in the
absence of explicit instructions (Klin et al., 2003). In fact, for
the above described studies, attending to and processing the
social, emotional or mentalizing aspects of the stimuli were
not explicit requirements of the task. For instance, in Pierce
et al. (2004), subjects were required simply to identify female
faces, regardless of whether they were familiar or not.
In Kennedy et al. (2006), subjects were asked only to count
Received 25 July 2007; Accepted 20 March 2008
Advance Access publication 28 April 2008
We thank Dr Cindy Carter for clinical assessment, Graham Wideman and Stephanie Carapetian for technical
assistance with stimulus presentation, Doreen Nguyen for assistance with data collection, Elizabeth Redcay and
Graham Wideman for helpful discussions and the researchers and staff at the UCSD Center for Functional MRI.
We also thank the participants and their families for graciously giving their time to take part in this study.
This research was supported by National Institutes of Health (RO1 MH36840 to E.C.).
Correspondence should be addressed to Daniel P. Kennedy, Division of Humanities and Social Sciences,
California Institute of Technology, HSS 228-77, Pasadena, CA 91125, USA. Email: kennedy@caltech.edu.
Present address: Daniel P. Kennedy, Division of Humanities and Social Sciences, California Institute of
Technology, HSS 228-77, Pasadena, CA 91125, USA.
doi:10.10 93/sc a n/nsn011 SCAN (2008) 3,17719 0
ß The Author (2008). Published by Oxford University Press. For Permissions, please email: journals.permissions@oxfordjournals.org
Page 1
the number of emotional or neutral words displayed on the
screen, rather than explicitly process the meaning of the
words. Lastly, in Castelli et al. (2002), subjects were asked to
describe what they observed, and were free to interpret the
meaning of the movements as either reflecting intentionality
or not (and, in fact, the autism group provided significantly
lower intentionality ratings than the control group). Thus, it
is possible that given explicit instructions and explicit per-
formance requirements regarding the social, emotional or
mentalizing aspects of such tasks, regions of the default
network may exhibit more typical patterns of activity in
autism.
In the current experiment, we used explicitly defined social
and introspective tasks to determine whether abnormality
of default network regions reflects task-specific or task-
independent dysfunction. To do so, we used a self- and other-
reflection task, which has been shown previously to robustly
activate regions of the default network, including the MPFC,
RSC/PCC and ANG (Fletcher et al., 1995; Gusnard et al.,
2001; Johnson et al., 2002; Kelley et al., 2002; Gallagher and
Frith, 2003; Ochsner et al., 2005). While being scanned, 13
autism and 12 control subjects read particular statements
about themselves or about a close other person (i.e. their
mother), and made judgments as to whether the statements
were true or false. Thus, the subjects’ task (i.e. making true/
false judgments about themselves or others) was directly
relevant to the experimental conditions of interest (i.e.
reflection on oneself and others), reducing the likelihood of
non-engagement in the mental processes of interest. We also
included two different types of self- and other-reflection
conditions(i) those regarding psychological personality
traits (which we term INTERNAL) and (ii) those regarding
observable external characteristics and behaviors (which we
term EXTERNAL)which allowed us to examine whether
there may be a selective impairment in one or the other type of
judgment. All person judgment conditions were compared to
a cognitively demanding MATH condition, which served as
an experimental baseline task. Finally, we included a resting
fixation condition (REST) to compare resting default network
activity between groups, to examine the overlap between
regions of the default network and brain regions involved in
self- and other-reflection, and to functionally define the
default network for use in region-of-interest analyses.
METHODS
Participants
Fourteen male autism spectrum disorder (ASD) and 13 male
control subjects were scanned. Due to excessive movement
during scanning, one ASD subject and one control subject
were removed from the analysis, resulting in a final sample
size of 13 ASD (six autism, six Asperger’s, one PDD-NOS)
and 12 control subjects. With the exception of the one subject
(A10, Table 1), this sample of control and ASD subjects
completely overlapped with those from a separate imaging
study that examined resting functional connectivity in autism
(Kennedy and Courchesne, 2008). Informed written consent
was obtained from all participants or, when appropriate, their
legal guardians, and all participants received monetary com-
pensation for their time. The protocol was approved by the
Institutional Review Board of UCSD and Children’s Hospital
at San Diego. ASD participants were diagnosed by a clinical
psychologist using the Autism Diagnostic InterviewRevised
(ADI-R) (Lord et al., 1994) and the Autism Diagnostic
Observation Schedule (ADOS) (Lord et al., 2000). Individuals
meeting the criteria for an ASD diagnosis but without early
spoken language delay and with average to above-average
IQ scores received the diagnosis of Asperger’s Syndrome.
The PDD-NOS subject did not meet the combined social and
communication cutoff score of 10 to warrant a diagnosis of
autism on the ADOS, nor did he meet the above criteria for
Asperger’s Syndrome. With the exception of one control
subject, IQ scores were obtained from all participants using
the Wechsler Adult Intelligence Scale (WAIS) or WAIS-R
(Revised). The mean age of the autism participants (26.9
years) and the control participants (27.5 years) was not
significantly different [t(23) ¼ 0.129, P > 0.85]. Subject
groups did not differ significantly in verbal, performance or
full-scale IQ [verbal: t(22) ¼ 1.641, P ¼ 0.115; performance:
t(22) ¼ 1.512, P ¼ 0.145; full-scale: t(22) ¼ 1.959, P ¼ 0.063].
See Table 1 for detailed clinical information.
Stimuli
While in the scanner, subjects made true/false judgments
for various statements about themselves (SELF condition) or
a close other person (OTHER condition). These SELF
and OTHER statements either referred to psychological
personality traits (INTERNAL condition) or to observable
external characteristics and behaviors (EXTERNAL condi-
tion). In all cases, the close other was their mother, with the
exception of one control subject who read statements about a
close friend rather than his mother, as his parents were
deceased. Thus, there were four person judgment
(i.e. MENTAL) conditions in total: INTERNAL-SELF
(e.g. ‘I am polite’), INTERNAL-OTHER (e.g. ‘My mother is
generous’), EXTERNAL-SELF (e.g. ‘I drink coffee’) and
EXTERNAL-OTHER (e.g. ‘My mother drives a car’) (see
Appendix A for a complete list of statements). A MATH
condition served as an experimental baseline condition,
wherein subjects were shown math equations [in the form of a
two-digit number plus a one-digit number equaling either a
correct or incorrect answer (e.g. ‘45 þ 8 ¼ 53’)], and again
instructed to respond via button presses as to whether the
equation was true or false. Finally, there was a REST condition
where subjects passively viewed a fixation cross that appeared
on the screen. The functional scans also included an episodic
memory judgment condition, but this condition was not
examined in the current analysis.
Each trial consisted of a statement, equation or fixation
cross shown for 2500 ms, followed by a blank screen for
500 m. Conditions were presented in a counterbalanced block
178 SCAN (2008) D. P. Kennedy and E. Courchesne
Page 2

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Default network activity in autism SCAN (2008) 189
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Appendix A Complete list of stimuli used in the present experiment. Statements for the OTHER condition
were modified by replacing ‘I’ with ‘My mother’ and modifying the verb appropriately (e.g., I am ...
becomes ‘My mother is ...’).
SELF, INTERNAL SELF, EXTERNAL
I am a quiet person I usually wear white socks
I am an emotional person I eat pizza often
I am a loving person I use computers often
I am generous I usually eat breakfast
I am a relaxed person I often make my bed
I am a good listener I drive on highways often
I am funny I drive a car
I am talkative I eat fruit often
I am polite I read books often
I am honest I eat at restaurants a lot
I am competitive I eat chicken often
I am a patient person I watch a lot of TV
I am a quick learner I go shopping often
I am friendly I drink coffee often
I am a moody person I talk on the phone a lot
I am a happy person I take showers in the morning
I am easily upset I go to the movies often
I am easily stressed I read the newspaper
I am a focused person I spend a lot of money
I am easily distracted I listen to music often
I am a demanding person I wash dishes
I am very thoughtful I talk to my family often
I am very observant I wear jeans often
I am a confident person I am a deep sleeper
I am a curious person I usually wake up early
I am compassionate I listen to the radio
I am a nurturing person I usually go to bed early
I am creative I take naps often
I am easily bored I usually cook dinner
I am easily scared I dance often
I am shy I go to the beach sometimes
I am dependable I read books often
I am kind I watch sports games
I am outgoing I swim sometimes
I am helpful I check my email often
I am sensitive I have a dog
I am hard-working I buy a lot of CDs
I am easily frustrated I eat burritos often
I am a silly person I go to the mall a lot
I am a caring person I drink juice often
I am lazy I go on walks often
I am a selfish person I rent a lot of movies
I am controlling I read magazines
I am a rude person I eat a lot of candy
I am respectful I go to the bank often
I am smart I play video games often
I am a serious person I work out a lot
I am easily disappointed I do my laundry often
190 SCAN (2008) D. P. Kennedy and E.Courchesne
Page 14
  • Source
    • "Autism spectrum conditions (henceforth, autism) are associated with deficits in social and self-referential information processing (Lombardo and Baron-Cohen 2011; Frith 2001; Williams 2010 ) and much neurological evidence points to the mPFC as an important site of dysfunction underpinning these characteristics (Ben Shalom 2009; Uddin 2011). Reduced mPFC activity has been reported in individuals with autism during tasks requiring mentalizing (Frith 2001; Murdaugh et al. 2012; White et al. 2014), with mPFC activity levels distinguishing less between 'self' and 'other' during self-reference and selfother judgement tasks than in typical individuals (Kennedy and Courchesne 2008; Lombardo et al. 2009), suggesting that representations of self-and other-related information may not be as distinct. Subtle memory deficits also exist in autism, largely consisting of impaired episodic memory but intact semantic memory (Boucher et al. 2012; Bowler et al. 2011). "
    [Show abstract] [Hide abstract] ABSTRACT: Studies of reality monitoring (RM) often implicate medial prefrontal cortex (mPFC) in distinguishing internal and external information, a region linked to autism-related deficits in social and self-referential information processing, executive function, and memory. This study used two RM conditions (self-other; perceived-imagined) to investigate RM and metamemory in adults with autism. The autism group showed a deficit in RM, which did not differ across source conditions, and both groups exhibited a self-encoding benefit on recognition and source memory. Metamemory for perceived-imagined information, but not for self-other information, was significantly lower in the autism group. Therefore, reality monitoring and metamemory, sensitive to mPFC function, appear impaired in autism, highlighting a difficulty in remembering and monitoring internal and external details of past events.
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    • "Our findings indicate a different pattern of interactions between the defaultmode and several sub-networks associated with sensorymotor, visual and executive processing in ASD. Abnormalities in the connectivity between nodes of the default-mode network (DMN) has been widely investigated in ASD ([3, 30, 50]) giving its associations with social cognition ([10]). There are also functional connectivity studies reporting ASD-related differences in motor and visual networks ([31, 33]). "
    [Show abstract] [Hide abstract] ABSTRACT: The global functional brain network (graph) is more suitable for characterizing brain states than local analysis of the connectivity of brain regions. Therefore, graph-theoretic approaches are the natural methods to study the brain. However, conventional graph theoretical analyses are limited due to the lack of formal statistical methods for estimation and inference for random graphs. For example, the concept of correlation between two vectors of graphs is yet not defined. The aim of this article to introduce a notion of correlation between graphs. In order to develop a framework to infer correlation between graphs, we assume that they are generated by mathematical models and that the parameters of the models are our random variables. Then, we define that two vectors of graphs are independent whether their parameters are independent. The problem is that, in real world, the model is rarely known, and consequently, the parameters cannot be estimated. By analyzing the graph spectrum, we showed that the spectral radius is highly associated with the parameters of the graph model. Based on it, we constructed a framework for correlation inference between graphs and illustrate our approach in a functional magnetic resonance imaging data composed of 814 subjects comprising 529 controls and 285 individuals diagnosed with autism spectrum disorder (ASD). Results show that correlations between default-mode and control, default-mode and somatomotor, and default-mode and visual sub-networks are higher ($p<0.05$) in ASD than in controls.
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    • "Whole-brain analyses for the primary DMN seed in PCC showed a distinct pattern, with a large underconnectivity cluster in mPFC, but extensive overconnectivity clusters across multiple occipital, parietal, and frontal regions bilaterally. Underconnectivity between PCC and mPFC (another major node of the DMN) has been observed in previous studies (Kennedy and Courchesne 2008; Monk et al. 2009; Assaf et al. 2010; Murdaugh et al. 2012; Starck et al. 2013; von dem Hagen et al. 2013; Washington et al. 2014; Doyle‐Thomas et al. 2015), being one of the most replicated findings in the ASD iFC literature (although it was not seen in our low-motion subsample, without GSR; SupplementaryFig. 3). "
    [Show abstract] [Hide abstract] ABSTRACT: Autism spectrum disorder (ASD) is characterized by atypical brain network organization, but findings have been inconsistent. While methodological and maturational factors have been considered, the network specificity of connectivity abnormalities remains incompletely understood. We investigated intrinsic functional connectivity (iFC) for four "core" functional networks-default-mode (DMN), salience (SN), and left (lECN) and right executive control (rECN). Resting-state functional MRI data from 75 children and adolescents (37 ASD, 38 typically developing [TD]) were included. Functional connectivity within and between networks was analyzed for regions of interest (ROIs) and whole brain, compared between groups, and correlated with behavioral scores. ROI analyses showed overconnectivity (ASD > TD), especially between DMN and ECN. Whole-brain results were mixed. While predominant overconnectivity was found for DMN (posterior cingulate seed) and rECN (right inferior parietal seed), predominant underconnectivity was found for SN (right anterior insula seed) and lECN (left inferior parietal seed). In the ASD group, reduced SN integrity was associated with sensory and sociocommunicative symptoms. In conclusion, atypical connectivity in ASD is network-specific, ranging from extensive overconnectivity (DMN, rECN) to extensive underconnectivity (SN, lECN). Links between iFC and behavior differed between groups. Core symptomatology in the ASD group was predominantly related to connectivity within the salience network.
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