Feedback-driven trial-by-trial learning in autism spectrum disorders

Abstract

Objective: Impairments in learning are central to autism spectrum disorders. The authors investigated the cognitive and neural basis of these deficits in young adults with autism spectrum disorders using a well-characterized probabilistic reinforcement learning paradigm.

Method: The probabilistic selection task was implemented among matched participants with autism spectrum disorders (N=22) and with typical development (N=25), aged 18-40 years, using rapid event-related functional MRI. Participants were trained to choose the correct stimulus in high-probability (AB), medium-probability (CD), and low-probability (EF) pairs, presented with valid feedback 80%, 70%, and 60% of the time, respectively. Whole-brain voxel-wise and parametric modulator analyses examined early and late learning during the stimulus and feedback epochs of the task.

Results: The groups exhibited comparable performance on medium- and low-probability pairs. Typically developing persons showed higher accuracy on the high-probability pair, better win-stay performance (selection of the previously rewarded stimulus on the next trial of that type), and more robust recruitment of the anterior and medial prefrontal cortex during the stimulus epoch, suggesting development of an intact reward-based working memory for recent stimulus values. Throughout the feedback epoch, individuals with autism spectrum disorders exhibited greater recruitment of the anterior cingulate and orbito-frontal cortices compared with individuals with typical development, indicating continuing trial-by-trial activity related to feedback processing.

Conclusions: Individuals with autism spectrum disorders exhibit learning deficits reflecting impaired ability to develop an effective reward-based working memory to guide stimulus selection. Instead, they continue to rely on trial-by-trial feedback processing to support learning dependent upon engagement of the anterior cingulate and orbito-frontal cortices.

FIGURE 1. The Probabilistic Selection Task^a

^aStimulus pairs and valid and invalid probabilities are presented (left), as well as a schematic of the probabilistic selection task, including the stimulus epoch, interstimulus interval, feedback epoch, and intertrial interval (right). Sec=seconds.

FIGURE 2. State-Space Learning Curves and Certainty Plots for the Autism Spectrum Disorders and Typically Developing Groups^a

^aThe bottom row consists of certainty plots depicting trials for which the probability of typical development > autism spectrum disorders exceeds 95% certainty and becomes significant (blue dotted line) or for which the probability of autism spectrum disorders > typical development exceeds 95% certainly (red dotted line). There were significant differences in typical development > autism for the AB pair on trials 2, 3, 6, 51–62, 75–77, and 85–96. For CD trials, there were significant differences in typical development > autism spectrum disorders on trials 22 and 37–40. For EF trials, there were significant differences in typical development > autism spectrum disorders on trial 56 and in autism spectrum disorders > typical development on trials 66–69. ASD=autism spectrum disorders; Pr=probability; TYP=typical development.

FIGURE 3. Group Differences in Neural Recruitment During the Stimulus Epoch^a

^aThe top panel (A) represents the learning curve analysis. Neural recruitment on AB trials in the early phase of the task was significantly greater in the typically developing group compared with the autism spectrum disorders group in the anterior and rostral prefrontal cortex at a family-wise error-corrected p value <0.05. The bottom panel (B) shows results of the canonical model. The typically developing group exhibited greater neural recruitment on all trials through both phases of the task in the superior and anterior regions of the prefrontal cortex at a family-wise error-corrected p value <0.05. Error bars represent standard deviations. ASD=autism spectrum disorders; BA=Brodmann’s area; TYP=typical development.

FIGURE 4. Group Differences in Neural Recruitment During the Feedback Epoch^a

^aThe autism spectrum disorders group exhibited greater neural recruitment than the typically developing group in the rostral anterior cingulate and the orbito-frontal cortex on all trials through the early- and late-feedback epochs of the task at a family-wise error-corrected p value <0.05. Error bars represent standard deviations. ASD=autism spectrum disorders; BA=Brodmann’s area; TYP=typical development.