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

The subthalamic nucleus (STN) of the basal ganglia appears to have a potent role in action and cognition. Anatomical and imaging studies show that different frontal cortical areas directly project to the STN via so-called hyperdirect pathways. This review reports some of the latest findings about such circuits, including simultaneous recordings from cortex and the STN in humans, single-unit recordings in humans, high-resolution fMRI, and neurocomputational modeling. We argue that a major function of the STN is to broadly pause behavior and cognition when stop signals, conflict signals, or surprise signals occur, and that the fronto-STN circuits for doing this, at least for stopping and conflict, are dissociable anatomically and in terms of their spectral reactivity. We also highlight recent evidence for synchronization of oscillations between prefrontal cortex and the STN, which may provide a preferential "window in time" for single neuron communication via long-range connections.

https://www.jneurosci.org/content/jneuro/36/45/11489.full.pdf

Frontosubthalamic Circuits for Control of Action and Cognition.

Inhibitory control enables humans to stop prepotent motor activity, and is commonly studied using go/no-go or stop-signal tasks. In stop-signal tasks, prepotent motor activity is elicited by delaying stop signals relative to go signals. In go/no-go tasks, however, trials include only one signal-go or no-go. Hence, prepotent motor activity has to be ensured differently-for example, by using rare no-go trials and short trial durations. However, a literature survey shows that ∼40% of studies use equiprobable go/no-go trials and ∼20% use long stimulus-stimulus intervals (> 4 s). It is unclear whether such slow-paced, equiprobable go/no-go tasks elicit prepotent motor activity and probe inhibitory control. We recorded EEG during four go/no-go tasks, varying in no-go probability and trial duration. We quantified prepotent motor activity on successfully inhibited no-go trials using the lateralized readiness potential. Only fast-paced go/no-go tasks with rare no-go trials reliably evoked such activity. We then used a stop-signal task and independent component analysis to isolate an established neural signature of inhibitory control, and investigated this signature's activity across the go/no-go tasks. Across tasks, increased prepotent motor activity on individual no-go trials was accompanied by greater frontocentral P3 amplitudes, confirming it as an index of inhibition. Crucially, this inhibition-related activity showed a 75% reduction in slow-paced, equiprobable go/no-go tasks compared to fast-paced, rare no-go versions. Therefore, since many common go/no-go task configurations do not reliably evoke prepotent motor activity, their inhibitory requirements are greatly reduced. This has major implications for the usage of go/no-go tasks in psychological experiments.

Prepotent motor activity and inhibitory control demands in different variants of the go/no-go paradigm

Beta oscillations (∼13 to 30 Hz) have been observed during many perceptual, cognitive, and motor processes in a plethora of brain recording studies. Although the function of beta oscillations (hereafter "beta" for short) is unlikely to be explained by any single monolithic description, we here discuss several convergent findings. In prefrontal cortex (PFC), increased beta appears at the end of a trial when working memory information needs to be erased. A similar "clear-out" function might apply during the stopping of action and the stopping of long-term memory retrieval (stopping thoughts), where increased prefrontal beta is also observed. A different apparent role for beta in PFC occurs during the delay period of working memory tasks: it might serve to maintain the current contents and/or to prevent interference from distraction. We confront the challenge of relating these observations to the large literature on beta recorded from sensorimotor cortex. Potentially, the clear-out of working memory in PFC has its counterpart in the postmovement clear-out of the motor plan in sensorimotor cortex. However, recent studies support alternative interpretations. In addition, we flag emerging research on different frequencies of beta and the relationship between beta and single-neuron spiking. We also discuss where beta might be generated: basal ganglia, cortex, or both. We end by considering the clinical implications for adaptive deep-brain stimulation.

https://www.jneurosci.org/content/jneuro/39/42/8231.full.pdf

Beta Oscillations in Working Memory, Executive Control of Movement and Thought, and Sensorimotor Function

The ability to detect and correct action errors is paramount to safe and efficient goal-directed 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.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/psyp.13041

An adaptive orienting theory of error processing.

Surprising events markedly affect behaviour and cognition, yet the underlying mechanism is unclear. Surprise recruits a brain mechanism that globally suppresses motor activity, ostensibly via the subthalamic nucleus (STN) of the basal ganglia. Here, we tested whether this suppressive mechanism extends beyond skeletomotor suppression and also affects cognition (here, verbal working memory, WM). We recorded scalp-EEG (electrophysiology) in healthy participants and STN local field potentials in Parkinson's patients during a task in which surprise disrupted WM. For scalp-EEG, surprising events engage the same independent neural signal component that indexes action stopping in a stop-signal task. Importantly, the degree of this recruitment mediates surprise-related WM decrements. Intracranially, STN activity is also increased post surprise, especially when WM is interrupted. These results suggest that surprise interrupts cognition via the same fronto-basal ganglia mechanism that interrupts action. This motivates a new neural theory of how cognition is interrupted, and how distraction arises after surprising events.

/pdf/surprise-disrupts-cognition-via-a-fronto-basal-ganglia-2z4rcaitez.pdf

Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism

From psychology to economics there has been substantial interest in how costs (e.g., delay, risk) are represented asymmetrically during decision-making when attempting to gain reward or to avoid punishment. For example, in decision-making under risk, individuals show a tendency to prefer to avoid punishment than to acquire the equivalent reward (loss aversion). Although the cost of physical effort has recently received significant attention, it remains unclear whether loss aversion exists during effort-based decision-making. On the one hand, loss aversion may be hardwired due to asymmetric evolutionary pressure on losses and gains and therefore exists across decision-making contexts. On the other hand, distinct brain regions are involved with different decision costs, making it questionable whether similar asymmetries exist. Here, we demonstrate that young healthy human participants (Females:Males=16:6) exhibit loss aversion during effort-based decision-making by exerting more physical effort in order to avoid punishment than to gain a same-size reward. Next, we show that medicated Parkinson9s disease (PD) patients (Females:Males=9:9) show a reduction in loss aversion compared to age-matched controls (Females:Males=11:9). Behavioural and computational analysis revealed that people with PD exerted similar physical effort in return for a reward, but were less willing to produce effort in order to avoid punishment. Therefore, loss aversion is present during effort-based decision-making and can be modulated by altered dopaminergic state. This finding could have important implications for our understanding of clinical disorders that show a reduced willingness to exert effort in the pursuit of reward. SIGNIFICANCE STATEMENT Loss aversion — preferring to avoid punishment than to acquire equivalent reward — is an important concept in decision-making under risk. However, little is known about whether loss aversion also exists during decisions where the cost is physical effort. This is surprising given that motor cost shapes human behaviour, and a reduced willingness to exert effort is a characteristic of many clinical disorders. Here, we show that healthy human individuals exert more effort to minimise punishment than to maximise reward (loss aversion). We also demonstrate that medicated Parkinson9s disease patients exert similar effort to gain reward but less effort to avoid punishment when compared with healthy age-matched controls. This indicates that dopamine-dependent loss aversion is crucial for explaining effort-based decision-making.

https://www.jneurosci.org/content/jneuro/40/3/661.full.pdf

Dopamine-Dependent Loss Aversion during Effort-Based Decision-Making.

From psychology to economics there has been substantial interest in how costs (e.g., delay, risk) are represented asymmetrically during decision-making when attempting to gain reward or to avoid punishment. For example, in decision-making under risk, individuals show a tendency to prefer to avoid punishment than to acquire the equivalent reward (loss aversion). Although the cost of physical effort has received significant recent attention due to the evaluation of motor costs being crucial in our daily decisions, it remains unclear whether loss aversion exists during effort-based decision-making. On the one hand, loss aversion may be hardwired due to asymmetric evolutionary pressure on losses and gains and therefore exists across decision-making contexts. On the other hand, distinct brain regions are involved with different decision costs, making it questionable whether similar asymmetries exist. Here, we demonstrate that young healthy participants exhibit loss aversion during effort-based decision-making by exerting more physical effort in order to avoid punishment than to gain a same-size reward. Next, we show that medicated Parkinson9s disease (PD) patients show a reduction in loss aversion compared to age-matched controls. Behavioural and computational analysis revealed that people with PD exerted similar physical effort in return for a reward, but were less willing to produce effort in order to avoid punishment. Therefore, loss aversion is present during effort-based decision-making and can be modulated by altered dopaminergic state. This finding could have important implications for our understanding of clinical disorders that show a reduced willingness to exert effort in the pursuit of reward.

/pdf/dopamine-dependent-loss-aversion-during-effort-based-4n1bw2kt93.pdf

Dopamine-dependent loss aversion during effort-based decision-making

Motor adaptation is a process by which the brain gradually reduces error induced by a predictable change in the environment, e.g., pointing while wearing prism glasses. It is thought to occur via largely implicit processes, though explicit strategies are also thought to contribute. Research suggests a role of the cerebellum in the implicit aspects of motor adaptation. Using non-invasive brain stimulation, we sought to investigate the involvement of the cerebellum in implicit motor adaptation in healthy participants. Inhibition of the cerebellum was attained through repetitive transcranial magnetic stimulation (rTMS), after which participants performed a visuomotor-rotation task while using an explicit strategy. Adaptation and aftereffects of the TMS group showed no difference in behaviour compared to a Sham stimulation group, therefore this study did not provide any further evidence of a specific role of the cerebellum in implicit motor adaptation. However, our behavioral findings replicate those in the seminal study by Mazzoni and Krakauer (2006).

/pdf/an-implicit-plan-still-overrides-an-explicit-strategy-during-2piao2o0gu.pdf

An Implicit Plan Still Overrides an Explicit Strategy During Visuomotor Adaptation Following Repetitive Transcranial Magnetic Stimulation of the Cerebellum

Sarah H. E. M. Voets

Papers

Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism

Dopamine-Dependent Loss Aversion during Effort-Based Decision-Making.

Dopamine-dependent loss aversion during effort-based decision-making

An Implicit Plan Still Overrides an Explicit Strategy During Visuomotor Adaptation Following Repetitive Transcranial Magnetic Stimulation of the Cerebellum