Response monitoring, repetitive behaviour and anterior cingulate abnormalities in autism spectrum disorders (ASD)

Abstract

Autism spectrum disorders (ASD) are characterized by inflexible and repetitive behaviour. Response monitoring involves evaluating the consequences of behaviour and making adjustments to optimize outcomes. Deficiencies in this function, and abnormalities in the anterior cingulate cortex (ACC) on which it relies, have been reported as contributing factors to autistic disorders. We investigated whether ACC structure and function during response monitoring were associated with repetitive behaviour in ASD. We compared ACC activation to correct and erroneous antisaccades using rapid presentation event-related functional MRI in 14 control and ten ASD participants. Because response monitoring is the product of coordinated activity in ACC networks, we also examined the microstructural integrity of the white matter (WM) underlying this brain region using diffusion tensor imaging (DTI) measures of fractional anisotropy (FA) in 12 control and 12 adult ASD participants. ACC activation and FA were examined in relation to Autism Diagnostic Interview-Revised ratings of restricted and repetitive behaviour. Relative to controls, ASD participants: (i) made more antisaccade errors and responded more quickly on correct trials; (ii) showed reduced discrimination between error and correct responses in rostral ACC (rACC), which was primarily due to (iii) abnormally increased activation on correct trials and (iv) showed reduced FA in WM underlying ACC. Finally, in ASD (v) increased activation on correct trials and reduced FA in rACC WM were related to higher ratings of repetitive behaviour. These findings demonstrate functional and structural abnormalities of the ACC in ASD that may contribute to repetitive behaviour. rACC activity following errors is thought to reflect affective appraisal of the error. Thus, the hyperactive rACC response to correct trials can be interpreted as a misleading affective signal that something is awry, which may trigger repetitive attempts at correction. Another possible consequence of reduced affective discrimination between error and correct responses is that it might interfere with the reinforcement of responses that optimize outcomes. Furthermore, dysconnection of the ACC, as suggested by reduced FA, to regions involved in behavioural control might impair on-line modulations of response speed to optimize performance (i.e. speed-accuracy trade-off) and increase error likelihood. These findings suggest that in ASD, structural and functional abnormalities of the ACC compromise response monitoring and thereby contribute to behaviour that is rigid and repetitive rather than flexible and responsive to contingencies. Illuminating the mechanisms and clinical significance of abnormal response monitoring in ASD represents a fruitful avenue for further research.

Cognitive flexibility in autism spectrum disorder: Explaining the inconsistencies?

“…These deficits can also be linked with performance monitoring difficulties. Performance monitoring (also referred to as response monitoring) involves the process of evaluating the consequences of behavior and making adjustments to optimize outcomes (Thakkar et al, 2008). This appears to be problematic for individuals with ASD Thakkar et al, 2008).…”

“…Performance monitoring (also referred to as response monitoring) involves the process of evaluating the consequences of behavior and making adjustments to optimize outcomes (Thakkar et al, 2008). This appears to be problematic for individuals with ASD Thakkar et al, 2008). Difficulties with performance monitoring in ASD have been proposed to result from structural and functional abnormalities in the anterior cingulate cortex (ACC), which were also related to higher ratings of repetitive behavior (Thakkar et al, 2008).…”

“…This appears to be problematic for individuals with ASD Thakkar et al, 2008). Difficulties with performance monitoring in ASD have been proposed to result from structural and functional abnormalities in the anterior cingulate cortex (ACC), which were also related to higher ratings of repetitive behavior (Thakkar et al, 2008). Given that individuals with ASD perform adequately on explicitly cued switching tasks but fail on the more implicit switching tasks, where they have to interpret their own errors as a cue for initiating the switch, we hypothesize that a core aspect of the cognitive flexibility impairments in ASD might rely on deficient monitoring, interpreting and adjusting their own behavior.…”

Abnormal Developmental Trajectories of White Matter in Autism - The Contribution of MRI

“…a very heterogeneous group. Consistent findings in these studies were reduced FA in the CC Lee et al, 2009;Shukla et al, 2010Shukla et al, , 2011b in the superior temporal gyrus (Cheung et al, 2009;Lee et al, 2007Lee et al, , 2009Shukla et al, 2011a); the anterior cingulate cortex (Cheng et al, 2010;Thakkar et al, 2008); the frontal lobe (Cheng et al, 2010;Shukla etl al., 2011a;Sundaram et al, 2008); the thalamus (Lee et al, 2009) and the interior and posterior limbs of the internal capsule (Cheng et al, 2010;Shukla et al, 2010). (Catani et al, 2008).…”

Structural Neural Phenotype of Autism: Preliminary Evidence from a Diffusion Tensor Imaging Study Using Tract-Based Spatial Statistics

“…[8][9][10][11] Finally, there are now many DTI studies that have consistently demonstrated abnormalities in FA in the brains of ASD participants. [12][13][14][15][16][17] Because FA is a widely accepted measure of the structural integrity of white matter, 18 these studies have collectively demonstrated a pattern of findings consistent with neural disconnectivity in ASD. However, given the significant heterogeneity in methodologies and participants in these studies, it is difficult to identify a common underlying pattern of neuropathology across all studies.…”