Prediction-error signals in anterior cingulate cortex drive task-switching

Abstract

Task-switching is a fundamental cognitive ability which requires animals to update their knowledge of current rules, allowing flexible behaviour in a changing environment1. This is often achieved through evaluating discrepancies between observed and expected events. The anterior cingulate cortex (ACC) has a key role in processing such discrepancies, or prediction errors2–12. However, the neural circuit mechanisms underlying task-switching are largely unknown. Here we show that activity in the ACC induced by the absence of expected stimuli is necessary for rapid task-switching. Mice trained to perform a block-wise set-shifting task typically required a single experience of an expectation violation, or prediction error to accurately switch between responding to the same stimuli using distinct rules. Neurons in the ACC explicitly represented these prediction errors, and their activity was predictive of successful one-shot behavioural transitions. Prediction error signals were projection targetspecific, constrained in their spatio-temporal spread across cortex, and heavily disrupted by VIP interneuron perturbation. Optogenetic silencing and single-trial un-silencing revealed that the requirement of the ACC in task-switching was restricted to the epochs when neural prediction error signals were observed. These results reveal a dedicated circuitry promoting the transition between distinct cognitive states.

Fast updating feedback from piriform cortex to the olfactory bulb relays multimodal reward contingency signals during rule-reversal

“…The decoding analyses were successful even when zooming into arbitrarily chosen individual (~ 50 x 50 µm) fields of view, revealing robust representations of the task features in the cortical feedback activity. Across multiple rule-reversals within the same session, the neural ensembles transitioned fast back-and-forth between rule-associated representations, akin to reports in other brain regions 106,[116][117][118][119] . A given stimulus triggered similar cortical feedback activity in blocks of trials of the same contingency rule, and dissimilar representations in blocks of the opposite reward contingency, revealing attractor-like behavior in the piriform-to-bulb neural dynamics.…”

“…1d, Supplementary Figs. 1c,d) and completed an average of 5.8 ± 0.87 reversals (blocks of ~ 45 trials) per session, akin to other task-switching paradigms 106 . We used a stable 80% session performance as the criterion for 'expert' behavior and the starting point to monitor the cortical bulbar feedback activity (N = 7 mice, Methods, Figs.…”

Dynamic changes in somatosensory and cerebellar activity mediate temporal recalibration of self-touch

“…The anterior cingulate cortex showed gradually increasing activity to nondelayed selfgenerated touches during the adaptation session. The ACC has long been implicated in monitoring and resolving cognitive errors 126 , detecting response conflict [77][78][79][80][81] , computing prediction errors 82 , and signaling the unexpectedness of the outcomes of an action 83 . Activity in the ACC has been previously reported when investigating adaptation to temporal delays between voluntary taps and subsequently delivered light flashes 33 .…”

“…Second, given the involvement of the cerebellum in acquiring, storing, and recalibrating the internal models, as well as in sensorimotor learning 16,25,[69][70][71][72][73][74][75][76] , we expected delay adaptation to produce plastic changes in cerebellar activity reflecting the temporal recalibration of the internal model. Third, we reasoned that once the internal model has been recalibrated to a certain extent and the participants' nondelayed self-touches are "treated" as more unexpected, these will elicit activity in areas involved in conflict monitoring, such as the anterior cingulate cortex 33,[77][78][79][80][81][82][83] . This would occur because the unexpected nondelayed self-touch is conflicting with a lifetime of experiencing (nondelayed) self-touches as fully predictable.…”