Monitoring of Self-Paced Action Timing and Sensory Outcomes After Lesions to the Orbitofrontal Cortex

Abstract

Anticipation, monitoring, and evaluation of the outcome of one's actions are at the core of proactive control. Individuals with lesions to OFC often demonstrate behaviors that indicate a lack of recognition or concern for the negative effects of their actions. Altered action timing has also been reported in these patients. We investigated the role of OFC in predicting and monitoring the sensory outcomes of self-paced actions. We studied patients with focal OFC lesions (n = 15) and healthy controls (n = 20) while they produced actions that infrequently evoked unexpected outcomes. Participants performed a self-paced, random generation task where they repeatedly pressed right and left buttons that were associated with specific sensory outcomes: a 1- and 2-kHz tone, respectively. Occasional unexpected action outcomes occurred (mismatch) that inverted the learned button–tone association (match). We analyzed ERPs to the expected and unexpected outcomes as well as action timing. Neither group showed post-mismatch slowing of button presses, but OFC patients had a higher number of fast button presses, indicating that they were inferior to controls at producing regularly timed actions. Mismatch trials elicited enhanced N2b-P3a responses across groups as indicated by the significant main effect of task condition. Planned within-group analyses showed, however, that patients did not have a significant condition effect, suggesting that the result of the omnibus analysis was driven primarily by the controls. Altogether, our findings indicate that monitoring of action timing and the sensory outcomes of self-paced actions as indexed by ERPs is impacted by OFC damage.

Altered hierarchical auditory predictive processing after lesions to the orbitofrontal cortex

“…It might therefore be in a privileged position to generate predictions based on contextual and temporal structure in the environment, allowing quick adaptation to new rules ( Stalnaker et al, 2015 ; Wilson et al, 2014 ). Moreover, studies on time perception ( Solbakk et al, 2021 ; Berlin et al, 2004 ) support the importance of an intact OFC in maintaining temporal information needed to sustain a stable map of task context for longer periods, ultimately optimizing predictions ( Schuck et al, 2016 ; Schuck et al, 2018 ). Our findings align with these reports, highlighting the OFC’s role in maintaining internal representations of auditory sequences and generating robust PE signals when deviations occur.…”

“… Løvstad et al, 2012 reported attenuation of the P3a to unexpected novel environmental sounds after damage to either lateral PFC (LPFC) or OFC. Moreover, Solbakk et al, 2021 showed that the N2b-P3a complex elicited by unexpected auditory sensory outcomes of self-initiated actions in OFC patients did not differ as clearly from the response to expected outcomes as for the healthy controls. Altogether, these findings indicate that OFC integrity might be necessary for the generation of the auditory MMN and P3a, and support the idea that the OFC is involved in predicting different types of perceptual events and outcomes, and in noticing violations of expectation.…”

Altered hierarchical auditory predictive processing after lesions to the orbitofrontal cortex

“…156 This makes OFC suitable for supporting the formation of predictions that define the current task by using contextual and temporal structure in the environment to allow old rules to be disregarded so that new ones can be rapidly acquired. 34, 35 Moreover, findings from lesion studies of time perception 102, 157, 158 proposed that an intact OFC plays a role in maintaining temporal information needed to sustain a stable map of task context for a longer time, which in turn is needed to optimize predictions. 33, 146 Our findings support the idea that an intact OFC is necessary for holding an internal representation of the entire pool of sequences of auditory stimuli, sufficient to generate vigorous PE signals when violations of prediction are detected.…”

“…127 It might therefore be in a privileged position to generate predictions based on contextual and temporal structure in the environment, allowing quick adaptation to new rules. 27,28 Moreover, studies on time perception 83,128 support the importance of an intact OFC in maintaining temporal information needed to sustain a stable map of task context for longer periods, ultimately optimizing predictions. 26,129 Our findings align with these reports, highlighting the OFC's role in maintaining internal representations of auditory sequences and generating robust PE signals when deviations occur.…”

“…92, 93, 101 Løvstad et al 101 reported attenuation of the P3a to unexpected novel environmental sounds after damage to either lateral PFC (lPFC) or OFC. Moreover, Solbakk et al 102 showed that the N2b-P3a complex elicited by unexpected auditory sensory outcomes of self-initiated actions in OFC patients did not differ as clearly from the response to expected outcomes as for the healthy controls. Altogether, these findings indicate that OFC integrity might be necessary for the generation of the auditory MMN and P3a and support the idea that the OFC is involved in predicting different types of perceptual events and outcomes, monitoring ensuing sensory inputs, as well as noticing and evaluating violations of expectation.…”