The Subthalamic Nucleus Contributes to Post-error Slowing

Cavanagh, James F.; Sanguinetti, Joseph L.; Allen, John J. B.; Sherman, Scott J.; Frank, Michael J.

doi:10.1162/jocn_a_00659

Cited by 47 publications

(53 citation statements)

References 44 publications

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“…Regarding the putative target of these frontal nodes, two other studies of PES recorded the STN-LFP in DBS patients (Cavanagh et al, 2014; Siegert et al, 2014). Both studies showed that STN activity was increased following errors, and related to PES on the next trial (the studies differ slightly in the time window at which they identify STN activity that predicts PES; Siegert et al showed that the phase-locked LFP at around 300ms following the erroneous response correlated with PES, while Cavanagh et al showed that the event-related spectral perturbations in the theta frequency immediately before the next response related to PES).…”

Section: Role Of Global Stopping Network In Slowing After Unexpected mentioning

confidence: 99%

On the Globality of Motor Suppression: Unexpected Events and Their Influence on Behavior and Cognition

Wessel

Aron

2017

Neuron

377

382

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SUMMARY Unexpected events are part of everyday experience. They come in several varieties – action errors, unexpected action outcomes, and unexpected perceptual events – and they lead to motor slowing and cognitive distraction. While different varieties of unexpected events have been studied largely independently, and many different mechanisms are thought to explain their effects on action and cognition, we suggest a unifying theory. We propose that unexpected events recruit a fronto-basal-ganglia network for stopping. This network includes specific prefrontal cortical nodes and is posited to project to the subthalamic nucleus, with a putative global suppressive effect on basal-ganglia output. We argue that unexpected events interrupt action and impact cognition, partly at least, by recruiting this global suppressive network. This provides a common mechanistic basis for different types of unexpected events, links the literatures on motor inhibition, performance-monitoring, attention, and working memory, and is relevant for understanding clinical symptoms of distractibility and mental inflexibility.

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Section: Role Of Global Stopping Network In Slowing After Unexpected mentioning

confidence: 99%

On the Globality of Motor Suppression: Unexpected Events and Their Influence on Behavior and Cognition

Wessel

Aron

2017

Neuron

377

382

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“…For example, EEG signatures that index successful motor inhibition in stop‐signal‐type tasks (Kok, Ramautar, De Ruiter, Band, & Ridderinkhof, ; Wessel & Aron, ) share neural generators with parts of the neural activity after errors (Wessel, ; Wessel & Aron, ; Wessel, Jenkinson et al, ), which suggests that they have a common neural generator (Onton, Westerfield, Townsend, & Makeig, ; Wessel, ). Furthermore, the subcortical STN, a core part of the purported inhibitory function of the frontobasal ganglia network, exhibits increased local field potential activity after errors (Cavanagh, Sanguinetti, Allen, Sherman, & Frank, ; Siegert et al, ) and unexpected events in general (Bockova et al, ; Wessel, Jenkinson et al, ). Lastly, just like action stopping (N. Swann et al, ), both action errors and unexpected action outcomes show increased frontocentral to right frontolateral beta‐frequency EEG coherence (Wessel, Ullsperger et al, ).…”

Section: Section Iii: An Adaptive Orienting Theory Of Error Processingmentioning

confidence: 99%

An adaptive orienting theory of error processing

2017

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The ability to detect and correct action errors is paramount to safe and efficient goaldirected behaviors. Existing work on the neural underpinnings of error processing and post-error behavioral adaptations has led to the development of several mechanistic theories of error processing. These theories can be roughly grouped into adaptive and maladaptive theories. While adaptive theories propose that errors trigger a cascade of processes that will result in improved behavior after error commission, maladaptive theories hold that error commission momentarily impairs behavior. Neither group of theories can account for all available data, as different empirical studies find both impaired and improved post-error behavior. This article attempts a synthesis between the predictions made by prominent adaptive and maladaptive theories. Specifically, it is proposed that errors invoke a nonspecific cascade of processing that will rapidly interrupt and inhibit ongoing behavior and cognition, as well as orient attention toward the source of the error. It is proposed that this cascade follows all unexpected action outcomes, not just errors. In the case of errors, this cascade is followed by error-specific, controlled processing, which is specifically aimed at (re) tuning the existing task set. This theory combines existing predictions from maladaptive orienting and bottleneck theories with specific neural mechanisms from the wider field of cognitive control, including from error-specific theories of adaptive post-error processing. The article aims to describe the proposed framework and its implications for post-error slowing and post-error accuracy, propose mechanistic neural circuitry for post-error processing, and derive specific hypotheses for future empirical investigations. K E Y W O R D Sattention, cognitive control, error processing, inhibitory control, orienting, performance monitoring | IN TRO DUCT IO NThe ability to adapt behavior after erroneous actions is one of the key components of human cognitive control. Correcting current and avoiding future errors is paramount to survival. These abilities are the centerpiece of the scientific field of performance monitoring. Research into the neurophysiological and behavioral changes associated with error processing has generated several influential theories over the past few decades, which seek to explain how the human brain reacts to error commission. While many existing theories entail unique mechanisms and propose specific corollaries, one factor by which all theories can be roughly classified is whether they propose that psychological and neural processes triggered by error commission are maladaptive or adaptive. Empirically, this classification can be made based on whether a theory predicts that error commission is ultimately beneficial or detrimental to post-error behavior. Specifically, adaptive theories propose that errors trigger a cascade of neural processes that represents a remedial effort of the cognitive system, which is explicitly targeted at avoiding f...

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“…In addition to this rapid cortically-mediated form of adaptation, evidence suggests that strategic adjustments in decision threshold are achieved via activity-dependent plasticity in the connections between STN and GPe [24,58] . In the current study, adaptive changes in the boundary height accounted for the observed post-error slowing in responses following failed stop trials, motivated by neuroimaging and electrophysiological evidence STN-mediated slowing of responses [9,17,26] . For simplicity, boundary adaption was restricted to being unidirectional -increasing after a stop-error and decaying back to, but never below, its original value.…”

Section: Drift-rate: Dopaminergic Modulation Of Corticostriatal Pathwaysmentioning

confidence: 95%

Errors in action timing and inhibition facilitate learning by tuning distinct mechanisms in the underlying decision process

Dunovan¹,

Verstynen²

2017

Preprint

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Goal-directed behavior requires integrating action selection processes with learning systems that adapt control using environmental feedback. These functions intersect in the basal ganglia (BG), which has at least two targets of plasticity: a dopaminergic modulation of striatal pathways and cortical modulation of the subthalamic nucleus (STN). Dual learning mechanisms suggests that feedback signals have a multifaceted impact on BG-dependent decisions. Using a hybrid of accumulation-to-bound decision models and reinforcement learning, we modeled the performance of humans in a stop-signal task where participants (N=75) learned the prior distribution of the timing of a stop signal through trial-and-error feedback. Changes in the drift-rate of the action execution process were driven by errors in action timing, whereas adaptation in the boundary height served to increase caution following failed stops. These findings highlight two interactive learning mechanisms for adapting the control of goal-directed actions based on dissociable dimensions of feedback error. . CC-BY4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/153676 doi: bioRxiv preprint first posted online Jun. 22, 2017; Author SummaryMany complex behavioral goals rely on one's ability to regulate the timing of action execution while also maintaining enough control to cancel actions in response to "Stop" cues in the environment. Here we examined how these two fundamental components of behavior become tuned to the control demands of the environment by combining principles of reinforcement learning with accumulator models of decision making. The synthesis of these two theoretical frameworks is motivated by previous work showing that reinforcement learning and control rely on overlapping circuitry in the basal ganglia. Leveraging knowledge about the interaction of learning and control signals in this network, we formulated a computational model in which performance feedback is used to modulate key mechanisms of the decision process to facilitate goal acquisition. Model-based analysis of behavioral data collected on an adaptive stop-signal task revealed two critical learning mechanisms: one that adjusts the accumulation rate of the "Go" signal to errors in action timing and another that exercises caution by raising the height of the execution boundary after a failed Stop trial. We show how these independent learning mechanisms interact over the course of learning, shedding light on the behavioral effects plasticity in different pathways of the basal ganglia.

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The Subthalamic Nucleus Contributes to Post-error Slowing

Cited by 47 publications

References 44 publications

On the Globality of Motor Suppression: Unexpected Events and Their Influence on Behavior and Cognition

On the Globality of Motor Suppression: Unexpected Events and Their Influence on Behavior and Cognition

An adaptive orienting theory of error processing

Errors in action timing and inhibition facilitate learning by tuning distinct mechanisms in the underlying decision process

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