Controlling Your Impulses: Electrical Stimulation of the Human Supplementary Motor Complex Prevents Impulsive Errors

To err is human. However, an inappropriate urge does not always result in error. Impulsive errors thus entail both a motor system capture by an urge to act and a failed inhibition of that impulse. Here we show that neuromodulatory electrical stimulation of the supplementary motor complex in healthy humans leaves action urges unchanged but prevents them from turning into overt errors. Subjects performed a choice reaction-time task known to trigger impulsive responses, leading to fast errors that can be revealed by analyzing accuracy as a function of poststimulus time. Yet, such fast errors are only the tip of the iceberg: electromyography (EMG) revealed fast subthreshold muscle activation in the incorrect response hand in an even larger proportion of overtly correct trials, revealing covert response impulses not discernible in overt behavior. Analyzing both overt and covert response tendencies enables to gauge the ability to prevent these incorrect impulses from turning into overt action errors. Hyperpolarizing the supplementary motor complex using transcranial direct current stimulation (tDCS) preserves action impulses but prevents their behavioral expression. This new combination of detailed behavioral, EMG, and tDCS techniques clarifies the neurophysiology of impulse control, and may point to avenues for improving impulse control deficits in various neurologic and psychiatric disorders

Immaturities in Reward Processing and Its Influence on Inhibitory Control in Adolescence

The nature of immature reward processing and the influence of rewards on basic elements of cognitive control during adolescence are currently not well understood. Here, during functional magnetic resonance imaging, healthy adolescents and adults performed a modified antisaccade task in which trial-by-trial reward contingencies were manipulated. The use of a novel fast, event-related design enabled developmental differences in brain function underlying temporally distinct stages of reward processing and response inhibition to be assessed. Reward trials compared with neutral trials resulted in faster correct inhibitory responses across ages and in fewer inhibitory errors in adolescents. During reward trials, the blood oxygen level–dependent signal was attenuated in the ventral striatum in adolescents during cue assessment, then overactive during response preparation, suggesting limitations during adolescence in reward assessment and heightened reactivity in anticipation of reward compared with adults. Importantly, heightened activity in the frontal cortex along the precentral sulcus was also observed in adolescents during reward-trial response preparation, suggesting reward modulation of oculomotor control regions supporting correct inhibitory responding. Collectively, this work characterizes specific immaturities in adolescent brain systems that support reward processing and describes the influence of reward on inhibitory control. In sum, our findings suggest mechanisms that may underlie adolescents’ vulnerability to poor decision-making and risk-taking behavior

The Neural Basis of Following Advice

Learning by following explicit advice is fundamental for human cultural evolution, yet the neurobiology of adaptive social learning is largely unknown. Here, we used simulations to analyze the adaptive value of social learning mechanisms, computational modeling of behavioral data to describe cognitive mechanisms involved in social learning, and model-based functional magnetic resonance imaging (fMRI) to identify the neurobiological basis of following advice. One-time advice received before learning had a sustained influence on people's learning processes. This was best explained by social learning mechanisms implementing a more positive evaluation of the outcomes from recommended options. Computer simulations showed that this “outcome-bonus” accumulates more rewards than an alternative mechanism implementing higher initial reward expectation for recommended options. fMRI results revealed a neural outcome-bonus signal in the septal area and the left caudate. This neural signal coded rewards in the absence of advice, and crucially, it signaled greater positive rewards for positive and negative feedback after recommended rather than after non-recommended choices. Hence, our results indicate that following advice is intrinsically rewarding. A positive correlation between the model's outcome-bonus parameter and amygdala activity after positive feedback directly relates the computational model to brain activity. These results advance the understanding of social learning by providing a neurobiological account for adaptive learning from advice

Conflict in object affordance revealed by grip force

Viewing objects can result in automatic, partial activation of motor plans associated with them—“object affordance”. Here, we recorded grip force simultaneously from both hands in an object affordance task to investigate the effects of conflict between coactivated responses. Participants classified pictures of objects by squeezing force transducers with their left or right hand. Responses were faster on trials where the object afforded an action with the same hand that was required to make the response (congruent trials) compared to the opposite hand (incongruent trials). In addition, conflict between coactivated responses was reduced if it was experienced on the preceding trial, just like Gratton adaptation effects reported in “conflict” tasks (e.g., Eriksen flanker). This finding suggests that object affordance demonstrates conflict effects similar to those shown in other stimulus–response mapping tasks and thus could be integrated into the wider conceptual framework on overlearnt stimulus–response associations. Corrected erroneous responses occurred more frequently when there was conflict between the afforded response and the response required by the task, providing direct evidence that viewing an object activates motor plans appropriate for interacting with that object. Recording continuous grip force, as here, provides a sensitive way to measure coactivated responses in affordance tasks

Lifespan development of stimulus-response conflict cost: similarities and differences between maturation and senescence

Age gradient of the mechanism of stimulus-response conflict cost was investigated in a population-based representative sample of 291 individuals, covering the age range from 6 to 89 years. Stimulus-response conflict cost, indicated by the amount of additional processing time required when there is a conflict between stimulus and response options, follows a U-shaped function across the lifespan. Lifespan age gradient of conflict cost parallels closely those of processing fluctuation and fluid intelligence. Individuals at both ends of the lifespan displayed a greater amount of processing fluctuation and at the same time a larger amount of conflict cost and a lower level of fluid intelligence. After controlling for chronological age and baseline processing speed, conflict cost continues to correlate significantly with fluid intelligence in adulthood and old age and with processing fluctuation in old age. The relation between processing fluctuation and conflict cost in old age lends further support for the neuromodulation of neuronal noise theory of cognitive aging as well as for theories of dopaminergic modulation of conflict monitoring

A consensus guide to capturing the ability to inhibit actions and impulsive behaviors in the stop-signal task

© Verbruggen et al. Response inhibition is essential for navigating everyday life. Its derailment is considered integral to numerous neurological and psychiatric disorders, and more generally, to a wide range of behavioral and health problems. Response-inhibition efficiency furthermore correlates with treatment outcome in some of these conditions. The stop-signal task is an essential tool to determine how quickly response inhibition is implemented. Despite its apparent simplicity, there are many features (ranging from task design to data analysis) that vary across studies in ways that can easily compromise the validity of the obtained results. Our goal is to facilitate a more accurate use of the stop-signal task. To this end, we provide 12 easy-to-implement consensus recommendations and point out the problems that can arise when they are not followed. Furthermore, we provide user-friendly open-source resources intended to inform statistical-power considerations, facilitate the correct implementation of the task, and assist in proper data analysis

Conscious perception of errors and its relation to the anterior insula

To detect erroneous action outcomes is necessary for flexible adjustments and therefore a prerequisite of adaptive, goal-directed behavior. While performance monitoring has been studied intensively over two decades and a vast amount of knowledge on its functional neuroanatomy has been gathered, much less is known about conscious error perception, often referred to as error awareness. Here, we review and discuss the conditions under which error awareness occurs, its neural correlates and underlying functional neuroanatomy. We focus specifically on the anterior insula, which has been shown to be (a) reliably activated during performance monitoring and (b) modulated by error awareness. Anterior insular activity appears to be closely related to autonomic responses associated with consciously perceived errors, although the causality and directions of these relationships still needs to be unraveled. We discuss the role of the anterior insula in generating versus perceiving autonomic responses and as a key player in balancing effortful task-related and resting-state activity. We suggest that errors elicit reactions highly reminiscent of an orienting response and may thus induce the autonomic arousal needed to recruit the required mental and physical resources. We discuss the role of norepinephrine activity in eliciting sufficiently strong central and autonomic nervous responses enabling the necessary adaptation as well as conscious error perception