Feedback and reward processing in high-functioning autism
Introduction
Individuals with Autism Spectrum Disorders (ASD) frequently display social, cognitive, and behavioral deficits that result from the consequences of atypical brain development and altered interactions with the environment. Several studies of the cognitive associations of social dysfunction in individuals diagnosed with ASD report limitations in the ability to process social stimuli, feedback, and reward. For example, Dawson et al. (2001) found that poor performance in individuals with ASD on a delayed non-matching to sample task appeared to arise from a difficulty in forming abstract stimulus–reward associations rather than deficits in visual object recognition. Ingersoll et al. (2003) found that young children diagnosed with autism better imitated the use of toys that were associated with concrete sensory feedback than abstract social feedback. Such difficulties in feedback and reward processing are thought to be the result of dysfunction of the fronto-striatal reward system, which may place greater emphasis on cognitive rather than emotional aspects of feedback (Schmitz et al., 2008).
The neural underpinnings of feedback and reward processing can be measured using the feedback-related negativity (FRN) component of the scalp-recorded event-related potential (ERP). The FRN is a negative deflection in the ERP that occurs approximately 250 ms to 300 ms following the presentation of feedback and is more negative to losses or unexpected outcomes than gains or expected outcomes (e.g., Gehring and Willoughby, 2002, Holroyd et al., 2003, Hajcak et al., 2006). More broadly speaking, the FRN represents an electrophysiological reflection of whether a desired result has been achieved and may represent a mechanism for performance feedback-signaling for adjustments in behaviors when outcomes are not consistent with behaviors or expectations (Hajcak et al., 2006). Source localization studies of the FRN broadly implicate areas of the medial–frontal cortex, including the anterior cingulate cortex (ACC) as the neural generator (Gehring and Willoughby, 2002, Holroyd and Coles, 2002, Ruchsow et al., 2002, Nieuwenhuis et al., 2005), although additional areas such as the posterior cingulate, superior frontal gyrus, fusiform gyrus, and superior temporal gyrus have also been identified (e.g., van Veen et al., 2004, De Pascalis et al., 2010).
The FRN may be an important reflection of discrepancies between predicted and actual reward in the mesencephalic dopamine system. Dopaminergic activity in neurons connecting the basal ganglia and the ACC use reinforcement signals to promote feedback-based learning by processing negative events and determining suitable behavior for the given situation (Holroyd et al., 2003, Fein and Chang, 2008, Crowley et al., 2009). Disruption of the dopaminergic metabolism system involving the ACC, basal ganglia and prefrontal cortex may likewise contribute to behavioral deficits in ASD, by interfering with the ability to respond effectively to reward and punishment (Kendrick, 2004). Dopamine plays an important role in reward, sending error signals through neurons in the mesencephalic dopamine system to the ACC. These neurons aid in predicting the discrepancy between predicted and actual reward and are important in systems that code error and determine behavior (Holroyd et al., 2004, Crowley et al., 2009).
There is only one study published to date that relates to ASD and ERP components associated with feedback (Groen et al., 2008). Their study of a small sample (n = 17) of children diagnosed with subthreshold ASD did not show a typical FRN in individuals with ASD, individuals with attention-deficit hyperactivity disorder (ADHD), or typically developing (TD) children. However, they did find that ERPs associated with feedback anticipation and early feedback processing (e.g., the P2a waveform) did not reliably differ between TD children and those with subthreshold ASD. Groups did differ as a function of feedback valence on late P300 potentials associated with feedback processing. These differences possibly reflect an inability to integrate external error information into performance feedback (Groen et al., 2008). In addition, children with ASD showed greater anticipation for positive feedback throughout the task, in contrast to TD children. Overall, Groen et al. suggest that children with ASD may place greater significance on positive than negative feedback stimuli (see also Wilbarger et al., 2009); however, it is difficult to generalize from the results of this study as the FRN anticipated in their feedback task was not found and the sample consisted of individuals with subthreshold autism.
Several recent studies, including one conducted in our lab with an overlapping sample to those presented here, show reduced response amplitude on the error-related negativity (ERN) component of the ERP in individuals with ASD relative to controls (Vlamings et al., 2008, Sokhadze et al., 2010, South et al., 2010, Santesso et al., 2011). The ERN is an internal signal of error commission or conflict detection primarily found following errors on forced-choice reaction time tasks (see van Veen and Carter, 2006, for review). The ERN is reliably associated with emotional traits and processes, such as negative affect (Luu et al., 2000), anxiety and depression (Olvet and Hajcak, 2008), and even satisfaction with life (Larson et al., 2010). The FRN, on the other hand, is a reflection of more concrete processes and is based on external feedback that influences reinforcement-based learning and performance (Nieuwenhuis et al., 2004).
Prominent theories of the ERN and FRN suggest that these components both represent a reinforcement learning response to performance or feedback supported by the same mechanisms in the ACC (Holroyd and Coles, 2002). Studies directly comparing the two components, however, show mixed results. One study shows the ERN and FRN share a neural generator in the ACC, with an additional generator in the prefrontal cortex (Potts et al., 2011) and others showing nearly identical neural processes and generators (Heldmann et al., 2008, Gentsch et al., 2009). Regardless, studies suggest that these components are temporally dissociable, with one representing a response to concrete external feedback and the other representing an internally generated signal of a failure to reach expected outcomes (Gentsch et al., 2009).
The purpose of the present study was to examine the neural response to reward, as represented by the FRN, in individuals with ASD and typically developing controls. Our study adds to the previous study of the FRN in ASD conducted by Groen et al. (2008) by: a) using a task specifically intended to measure the FRN as a function of gains and losses; and, b) using a sample that meets stricter guidelines for ASD. Given performance monitoring and feedback decrements in individuals with autism, we hypothesized that individuals with ASD would show decreased-amplitude FRN values relative to healthy control participants.
Section snippets
Participants
All procedures were approved by the Institutional Review Board at Brigham Young University. Initial study enrollment included 26 individuals with ASD and 25 typically developing control participants. Data from one outlier participant with ASD were excluded due to means more than two standard deviations below the group averages for the FRN. The final sample, therefore, included 25 individuals with ASD between the ages of 9 and 21 years (M = 13.89 years, S.D. = 2.46; two female) and 25 age- and
Response times
As expected, mean RTs did not differ between individuals with ASD and controls on loss trials, t(48) = 0.25, p = 0.80, d = 0.07, or gain trials, t(48) = 0.16, p = 0.88, d = 0.04, indicating groups did not respond more impulsively or differentially to loss or gain trials. Participants with ASD had a mean (± S.D.) RT of 1419.40 (604.49) for loss trials and 1503.18 (627.76) for gain trials; controls had a mean RT of 1461.43 (577.92) for loss trials and 1529.81 (575.45) for gain trials.
Event-related potential data
Similar to the RT data,
Discussion
We did not find significant differences in FRN amplitude between our sample of 25 individuals diagnosed with ASD compared to 25 age- and IQ-matched typically developing controls. Our results generally replicate the only previously published study of the FRN in ASD conducted by Groen et al. (2008), although our sample was diagnostically more severe and our task was utilized more specifically to elicit and analyze the FRN component of the ERP. That is, neither study found consistent group
Acknowledgements
We gratefully acknowledge the assistance of Oliver Johnston and Peter Clayson in data collection. This study was supported by funds from the Brigham Young University College of Family, Home, and Social Sciences.
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These authors contributed equally and are considered co-first authors.