Human behaviour is generally guided by the anticipation of potential outcomes that are considered to be rewarding. Reward processing can thus be dissected into a phase of reward anticipation and a ...phase of reward consumption. A number of brain structures have been suggested to be involved in reward processing. However, it is unclear whether anticipation and consumption are mediated by the same or different neural networks. We examined the neural basis of these processes using functional magnetic resonance imaging (fMRI) in an incentive delay task offering either money or social approval. In both conditions participants (N=28) were given a cue indicating potential reward. In order to receive reward a target button had to be pushed within a certain time window (adapted for individual reaction time). Cues triggering either monetary or social reward anticipation were presented sessionwise. Imaging was performed on a 1.5-Tesla Philips scanner in an event-related design. Anticipation of both reward types activated brain structures constituting the brain reward system including the ventral striatum. In contrast to the task independent activity in the anticipation phase, reward consumption evoked different patterns of activation for money and social approval, respectively. While social stimuli were mainly associated with amygdala activation, the thalamus was more strongly activated by the presentation of monetary rewards. Our results identify dissociable neural networks for the anticipation and consumption of reward. The findings implicate that the neural mechanisms underlying reward consumption are more modality-specific than those for reward anticipation, and that they are mediated by subjective reward value.
Most behavioral training regimens in autism spectrum disorders (ASD) rely on reward-based reinforcement strategies. Although proven to significantly increase both cognitive and social outcomes and ...successfully reduce aberrant behaviors, this approach fails to benefit a substantial number of affected individuals. Given the enormous amount of clinical and financial resources devoted to behavioral interventions, there is a surprisingly large gap in our knowledge of the basic reward mechanisms of learning in ASD. Understanding the mechanisms for reward responsiveness and reinforcement-based learning is urgently needed to better inform modifications that might improve current treatments. The fundamental goal of this review is to present a fine-grained literature analysis of reward function in ASD with reference to a validated neurobiological model of reward: the 'wanting'/'liking' framework. Despite some inconsistencies within the available literature, the evaluation across three converging sets of neurobiological data (neuroimaging, electrophysiological recordings, and neurochemical measures) reveals good evidence for disrupted reward-seeking tendencies in ASD, particularly in social contexts. This is most likely caused by dysfunction of the dopaminergic-oxytocinergic 'wanting' circuitry, including the ventral striatum, amygdala, and ventromedial prefrontal cortex. Such a conclusion is consistent with predictions derived from diagnostic criteria concerning the core social phenotype of ASD, which emphasize difficulties with spontaneous self-initiated seeking of social encounters (that is, social motivation). Existing studies suggest that social 'wanting' tendencies vary considerably between individuals with ASD, and that the degree of social motivation is both malleable and predictive of intervention response. Although the topic of reward responsiveness in ASD is very new, with much research still needed, the current data clearly point towards problems with incentive-based motivation and learning, with clear and important implications for treatment. Given the reliance of behavioral interventions on reinforcement-based learning principles, we believe that a systematic focus on the integrity of the reward system in ASD promises to yield many important clues, both to the underlying mechanisms causing ASD and to enhancing the efficacy of existing and new interventions.
Neurobiological research in autism spectrum disorders (ASD) has paid little attention on brain mechanisms that cause and maintain restricted and repetitive behaviors and interests (RRBIs). Evidence ...indicates an imbalance in the brain's reward system responsiveness to social and non-social stimuli may contribute to both social deficits and RRBIs. Thus, this study's central aim was to compare brain responsiveness to individual RRBI (i.e., circumscribed interests), with social rewards (i.e., social approval), in youth with ASD relative to typically developing controls (TDCs).
We conducted a 3T functional magnetic resonance imaging (fMRI) study to investigate the blood-oxygenation-level-dependent effect of personalized circumscribed interest rewards versus social rewards in 39 youth with ASD relative to 22 TDC. To probe the reward system, we employed short video clips as reinforcement in an instrumental incentive delay task. This optimization increased the task's ecological validity compared to still pictures that are often used in this line of research.
Compared to TDCs, youth with ASD had stronger reward system responses for CIs mostly within the non-social realm (e.g., video games) than social rewards (e.g., approval). Additionally, this imbalance within the caudate nucleus' responsiveness was related to greater social impairment.
The current data support the idea of reward system dysfunction that may contribute to enhanced motivation for RRBIs in ASD, accompanied by diminished motivation for social engagement. If a dysregulated reward system indeed supports the emergence and maintenance of social and non-social symptoms of ASD, then strategically targeting the reward system in future treatment endeavors may allow for more efficacious treatment practices that help improve outcomes for individuals with ASD and their families.
Motivation for goal-directed behaviour largely depends on the expected value of the anticipated reward. The aim of the present study was to examine how different levels of reward value are coded in ...the brain for two common forms of human reward: money and social approval. To account for gender differences 16 male and 16 female participants performed an incentive delay task expecting to win either money or positive social feedback. fMRI recording during the anticipation phase revealed proportional activation of neural structures constituting the human reward system for increasing levels of reward, independent of incentive type. However, in men activation in the prospect of monetary rewards encompassed a wide network of mesolimbic brain regions compared to only limited activation for social rewards. In contrast, in women, anticipation of either incentive type activated identical brain regions. Our findings represent an important step towards a better understanding of motivated behaviour by taking into account individual differences in reward valuation.
Obsessive-compulsive disorder (OCD) is characterized by persistent, unwanted thoughts and repetitive actions. Such repetitive thoughts and/or behaviors may be reinforced either by reducing anxiety or ...by avoiding a potential threat or harm, and thus may be rewarding to the individual. The possible involvement of the reward system in the symptomatology of OCD is supported by studies showing altered reward processing in reward-related regions, such as the ventral striatum (VS) and the orbitofrontal cortex (OFC), in adults with OCD. However, it is not clear whether this also applies to adolescents with OCD.
Using functional magnetic resonance imaging, two sessions were conducted focusing on the anticipation and receipt of monetary reward (1) or loss (2), each contrasted to a verbal (control) condition. In each session, adolescents with OCD (n1=31/n2=26) were compared with typically developing (TD) controls (n1=33/ n2=31), all aged 10-19 years, during the anticipation and feedback phase of an adapted Monetary Incentive Delay task.
Data revealed a hyperactivation of the VS, but not the OFC, when anticipating both monetary reward and loss in the OCD compared to the TD group.
These findings suggest that aberrant neural reward and loss processing in OCD is associated with greater motivation to gain or maintain a reward but not with the actual receipt. The greater degree of reward 'wanting' may contribute to adolescents with OCD repeating certain actions more and more frequently, which then become habits (i.e., OCD symptomatology).
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Abnormal brain oscillatory activity has been found in autism spectrum disorders (ASD) and proposed as a potential biomarker. While several studies have investigated gamma oscillations in ASD, none ...have examined resting gamma power across multiple brain regions. This study investigated resting gamma power using EEG in 15 boys with ASD and 18 age and intelligence quotient matched typically developing controls. We found a decrease in resting gamma power at right lateral electrodes in ASD. We further explored associations between gamma and ASD severity as measured by the Social Responsiveness Scale (SRS) and found a negative correlation between SRS and gamma power. We believe that our findings give further support of gamma oscillations as a potential biomarker for ASD.
Human social motivation is characterized by the pursuit of social reward and the avoidance of social punishment. The ventral striatum/nucleus accumbens (VS/Nacc), in particular, has been implicated ...in the reward component of social motivation, i.e., the ‘wanting’ of social incentives like approval. However, it is unclear to what extent the VS/Nacc is involved in avoiding social punishment like disapproval, an intrinsically pleasant outcome. Thus, we conducted an event-related functional magnetic resonance imaging (fMRI) study using a social incentive delay task with dynamic video stimuli instead of static pictures as social incentives in order to examine participants’ motivation for social reward gain and social punishment avoidance. As predicted, the anticipation of avoidable social punishment (i.e., disapproval) recruited the VS/Nacc in a manner that was similar to VS/Nacc activation observed during the anticipation of social reward gain (i.e., approval). Stronger VS/Nacc activity was accompanied by faster reaction times of the participants to obtain those desired outcomes. This data support the assumption that dynamic social incentives elicit robust VS/Nacc activity, which likely reflects motivation to obtain social reward and to avoid social punishment. Clinical implications regarding the involvement of the VS/Nacc in social motivation dysfunction in autism and social phobia are discussed.
•The neural mechanisms of seeking social reward and avoiding social punishment were studied.•A ‘dynamic’ social incentive delay task was used to increase ecological validity.•Social punishment avoidance and social reward gain activated the nucleus accumbens.•Stronger nucleus accumbens reactivity was accompanied by faster reaction times.•Clinical implications for individuals with autism and social phobia are discussed.
Autism spectrum disorder (ASD) is defined by two essential features
– impaired social communication abilities, including deficits with
social reciprocity, nonverbal communication and establishing ...relationships, and
by the presence of restricted and repetitive behaviors and interests (RRBIs).
Social deficits get the majority of attention both in science and in the popular
media, but RRBIs are equally important in understanding autism. Although RRBIs
are also seen in typically developing preschoolers, as well as in other
psychiatric disorders such as obsessive-compulsive disorder, their impairing and
persisting character is a hallmark of ASD
1
.
Repetitive behaviors are among the first signs of ASD, with significant
elevations by the child's first birthday
2
. Individuals with ASD of all ages and
cognitive ability levels display RRBIs to variable degrees, with males usually
being more severely affected than females
3
. Caregivers of individuals with ASD commonly emphasize
that RRBIs are among the most challenging facets of the disorder on an everyday
basis
1
. They negatively
impact social, cognitive, family functioning and well-being, often leading to
increased levels of parental stress and negative parenting styles. While the
clinical description and natural history of RRBIs is becoming clear, an
understanding of the biological bases of this set of features has only recently
begun to emerge
4
. Better
insight into the ontogenesis of RRBIs and their underlying neurobiology is
needed not only to inform models of the etiology of ASD, but also to foster the
development of new interventions.
In this issue of Biological Psychiatry, Langen et al.
5
examine differences in the rate of basal
ganglia growth in ASD relative to typically developing children (TDC). Their
volumetric analyses focused on developmental trajectories of the ventral
striatum (with nucleus accumbens) and dorsal striatum (with caudate nucleus and
putamen). These components of the basal ganglia are the major subcortical
targets within the frontostriatal behavior control loops that are recognized as
likely subserving RRBIs
4
. This
current study is a follow up of this same group's earlier work showing
cross sectional differences in growth trajectory. While several labs have
previously reported enlargement of the caudate nucleus in ASD, this current
study is the first to make repeat morphology measurements, thus overcoming
limitations associated with cross sectional analyses. This study involved 86
seven to seventeen year old cases and controls who had 2 MRI anatomical scans
approximately 2 and a half years apart on average, allowing a direct test of
differential striatal growth. The rate of basal ganglia growth was correlated
with the severity of RRBIs as assessed by parent interview at the time of the
first MRI scan, corroborating earlier work on the role of the striatum in
repetitive behaviors among children with ASD.
Specifically the caudate nucleus showed a growth rate in ASD that was
twice as high as the growth rate in TDC (i.e., 4.6% vs. 2.3%).
This was independent of overall brain growth, use of psychotropic medications,
or other major confounds. Most importantly, more severe RRBIs early in life,
particularly insistence on sameness behaviors, such as avoiding trivial changes
in routines and environments as well as adhering to compulsions and rituals,
were related to faster striatal growth between average ages of about 9 and 12
year old, with large effect sizes (e.g., caudate nucleus: Cohen's
d
= 0.86). While Langen et al. discuss several
complementary explanations for their findings, they conclude that the divergent
trajectory of caudate development in relation to RRBIs most likely results from
early, and possibly continuing, patterns of repetitive behaviors that shape
striatal development – not the other way around.
This new set of data elegantly adds to the notion that the striatum plays
a central role in core ASD phenomenology
6
. However, one question lingers: what cause RRBIs, like
insistence on sameness, compulsions and rituals, to become such a force so as to
impact the growth trajectory of an evolutionarily ancient brain structure like
the caudate nucleus? This question ties in with a long-standing debate among
clinicians and scientists concerning the potential functions that the myriad of
RRBIs might serve in individuals with ASD. While several plausible ideas have
been advanced
7
, convincing
support for any specific one is lacking.
One hypothesis that is gaining increased research attention, however,
involves the effects of alterations of the balance between social and nonsocial
motivation in
reward circuitry
on RRBIs
8
. This model suggests that ASD is in part
a disorder of “behavioral dependency” to RRBIs because of the
rewarding effects they induce
1
.
Indeed, insistence on sameness and preoccupying restricted interests are
reported to be quite pleasurable by affected individuals
1
. The dorsal striatum with caudate
nucleus, in particular, is believed to mediate reward value for purposeful
actions
5
. Functional
imaging studies show that the brain's reward circuitry in ASD,
particularly striatum and ventral prefrontal cortices, selectively over-reacts
to objects that may comprise an intense special interest, whereas it
under-reacts to more typical desires such as social reward and money
6
. This may indicate that the
brain in ASD cares less for conventional rewards. It is not yet known if an
initial lack of social reward motivation opens the door for enhanced rewarding
effects of certain circumscribed objects, topics, and routines, or whether the
reverse is true – that the dominating reward effects of nonsocial
objects, topic and routines diminishes the reward value of social
engagement.
The rewarding effects of RRBIs are thought to be fueled by the preference
of those with ASD for predictability in their environment, where they can
exercise more control; social encounters are in many ways the antithesis of
this, as these are often rapid, hard to control and offer much more variable
reinforcement contingencies. When RRBIs are rewarding, their pursuit may be
strengthened through reinforcement mechanisms that progressively turn them into
rigid and strongly desired habits that are performed almost automatically with
little conscious oversight. With this heuristic model, RRBIs are
self-reinforcing, and they begin to hijack the normal developmental trajectory
of entire repertoires of behaviors. The dorsal (associative) striatum with
caudate nucleus dominates these processes
4
. Thus, an accelerated growth rate of the caudate related
to RRBIs, as reported by Langen et al.
5
, could reflect atypical brain specialization in
individuals with ASD
9
. From
early in life the caudate nucleus mediates habitual processes for a wide range
of different stimuli and contexts. Across development, however, the caudate may
become co-opted by the most rewarding aspects of the environment. This
interactive and self-sustaining biobehavioral process – in concert with
other mesocorticolimbic functions
4
– may shape the growth trajectory of the caudate
nucleus and strengthens the occurrence of RRBIs in ASD (
Figure 1
). On a day-to-day basis, RRBIs interfere with
social development and functioning as they may absorb resources typically
dedicated to other learning opportunities, including social ones
6
.
The observation that RRBIs in ASD involve plasticity of the caudate
nucleus – one major hub within the frontostriatal circuits that control
behavior – is a fascinating advance for our field. It brings us closer
to the neurobiological roots of how and why affected individuals develop and
maintain this set of challenging behaviors. Follow-up research will need to
address several issues to improve upon the approach of the Langen et al study.
One critical issue is that researchers need to use more precise behavioral
measurement tools
10
. This
could involve item rating scales with greater item density around key concepts,
as it is clear to all the ADI-R is sorely lacking in this regard. Also,
quantitative motion capture tools are now widely available; deploying these in
natural environments seems to us to be extremely promising adjuncts to standard
rating scales. Repeat behavioral measurement across time, in sync with repeat
brain measurement is an important next step that will enable better
characterization of the interplay between RRBIs and brain dynamics. In this
regard, multimodal imaging in the same sample is called for, as structural
imaging will surely only capture portions of the story. The findings by Langen
et al.
5
call attention to the
importance of RRBIs in autism. Because RRBIs may be rooted in the powerful
reward circuitries that motivate a great deal of behavior, strategically
targeting the role of reward mechanisms promises to improve treatment practices
for limiting the life interfering aspects of RRBIs among individuals with ASD
and their families.
Autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD) are two frequently co-occurring neurodevelopmental conditions that share certain symptomatology, including social ...difficulties. This presents practitioners with challenging (differential) diagnostic considerations, particularly in clinically more complex cases with co-occurring ASD and ADHD. Therefore, the primary aim of the current study was to apply a data-driven machine learning approach (support vector machine) to determine whether and which items from the best-practice clinical instruments for diagnosing ASD (ADOS, ADI-R) would best differentiate between four groups of individuals referred to specialized ASD clinics (i.e., ASD, ADHD, ASD + ADHD, ND = no diagnosis). We found that a subset of five features from both ADOS (clinical observation) and ADI-R (parental interview) reliably differentiated between ASD groups (ASD & ASD + ADHD) and non-ASD groups (ADHD & ND), and these features corresponded to the social-communication but also restrictive and repetitive behavior domains. In conclusion, the results of the current study support the idea that detecting ASD in individuals with suspected signs of the diagnosis, including those with co-occurring ADHD, is possible with considerably fewer items relative to the original ADOS/2 and ADI-R algorithms (i.e., 92% item reduction) while preserving relatively high diagnostic accuracy. Clinical implications and study limitations are discussed.
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