Helga A. Harsay

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.

Corticostriatal Connectivity Underlies Individual Differences in the Balance between Habitual and Goal-Directed Action Control

Why are some individuals more susceptible to the formation of inflexible habits than others? In the present study, we used diffusion tensor imaging to demonstrate that brain connectivity predicts individual differences in relative goal-directed and habitual behavioral control in humans. Specifically, vulnerability to habitual “slips of action” toward no-longer-rewarding outcomes was predicted by estimated white matter tract strength in the premotor cortex seeded from the posterior putamen (as well as by gray matter density in the posterior putamen as determined with voxel-based morphometry). In contrast, flexible goal-directed action was predicted by estimated tract strength in the ventromedial prefrontal cortex seeded from the caudate. These findings suggest that integrity of dissociable corticostriatal pathways underlies individual differences in action control in the healthy population, which may ultimately mediate vulnerability to impulse control disorders.

Functional Connectivity of the Striatum Links Motivation to Action Control in Humans

Motivation improves the efficiency of intentional behavior, but how this performance modulation is instantiated in the human brain remains unclear. We used a reward-cued antisaccade paradigm to investigate how motivational goals (the expectation of a reward for good performance) modulate patterns of neural activation and functional connectivity to improve preparation for antisaccade performance. Behaviorally, subjects performed better (faster and more accurate antisaccades) when they knew they would be rewarded for good performance. Reward anticipation was associated with increased activation in the ventral and dorsal striatum, and cortical oculomotor regions. Functional connectivity between the caudate nucleus and cortical oculomotor control structures predicted individual differences in the behavioral benefit of reward anticipation. We conclude that although both dorsal and ventral striatal circuitry are involved in the anticipation of reward, only the dorsal striatum and its connected cortical network is involved in the direct modulation of oculomotor behavior by motivational incentive.

Error awareness and salience processing in the oddball task: shared neural mechanisms

A body of work suggests similarities in the way we become aware of an error and process motivationally salient events. Yet, evidence for a shared neural mechanism has not been provided. A within subject investigation of the brain regions involved in error awareness and salience processing has not been reported. While the neural response to motivationally salient events is classically studied during target detection after longer target-to-target intervals in an oddball task and engages a widespread insula-thalamo-cortical brain network, error awareness has recently been linked to, most prominently, anterior insula cortex. Here we explore whether the anterior insula activation for error awareness is related to salience processing, by testing for activation overlap in subjects undergoing two different task settings. Using a within subjects design, we show activation overlap in six major brain areas during aware errors in an antisaccade task and during target detection after longer target-to-target intervals in an oddball task: anterior insula, anterior cingulate, supplementary motor area, thalamus, brainstem, and parietal lobe. Within subject analyses shows that the insula is engaged in both error awareness and the processing of salience, and that the anterior insula is more involved in both processes than the posterior insula. The results of a fine-grained spatial pattern overlap analysis between active clusters in the same subjects indicates that even if the anterior insula is activated for both error awareness and salience processing, the two types of processes might tend to activate non-identical neural ensembles on a finer-grained spatial level. Together, these outcomes suggest a similar functional phenomenon in the two different task settings. Error awareness and salience processing share a functional anatomy, with a tendency toward subregional dorsal and ventral specialization within the anterior insula.

On the need of objective vigilance monitoring: effects of sleep loss on target detection and task-negative activity using combined EEG/fMRI

Sleep loss affects attention by reducing levels of arousal and alertness. The neural mechanisms underlying the compensatory efforts of the brain to maintain attention and performance after sleep deprivation (SD) are not fully understood. Previous neuroimaging studies of SD have not been able to separate the effects of reduced arousal from the effects of SD on cerebral responses to cognitive challenges. Here, we used a simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) approach to study the effects of 36 h of total sleep deprivation (TSD). Specifically, we focused on changes in selective attention processes as induced by an active acoustic oddball task, with the ability to isolate runs with objective EEG signs of high (SDalert) or reduced (SDsleepy) vigilance. In the SDalert condition, oddball task-related activity appears to be sustained by compensatory co-activation of insular regions, but task-negative activity in the right posterior node of the default mode network is altered following TSD. In the SDsleepy condition, oddball task-positive activity was massively impaired, but task-negative activation was showing levels comparable with the control condition after a well-rested night. Our results suggest that loss of strict negative correlation between oddball task-positive and task-negative activation reflects the effects of TSD, while the actual state of vigilance during task performance can affects either task-related or task-negative activity, depending on the exact vigilance level.

Remedial effects of motivational incentive on declining cognitive control in healthy aging and Parkinson's disease

The prospect of reward may provide a motivational incentive for optimizing goal-directed behavior. Animal work demonstrates that reward-processing networks and oculomotor-control networks in the brain are connected through the dorsal striatum, and that reward anticipation can improve oculomotor control via this nexus. Due perhaps to deterioration in dopaminergic striatal circuitry, goal-directed oculomotor control is subject to decline in healthy seniors, and even more in individuals with Parkinsons disease (PD). Here we examine whether healthy seniors and PD patients are able to utilize reward prospects to improve their impaired antisaccade performance. Results confirmed that oculomotor control declined in PD patients compared to healthy seniors, and in healthy seniors compared to young adults. However, the motivational incentive of reward expectation resulted in benefits in antisaccade performance in all groups alike. These findings speak against structural and non-modifiable decline in cognitive control functions, and emphasize the remedial potential of motivational incentive mechanisms in healthy as well as pathological aging.

Individual differences in risky decision-making among seniors reflect increased reward sensitivity

Increasing age is associated with subtle but meaningful changes in decision-making. It is unknown, however, to what degree these psychological changes are reflective of age-related changes in decision quality. Here, we investigated the effect of age on latent cognitive processes associated with risky decision-making on the Balloon Analog Risk Task (BART). In the BART, participants repetitively inflate a balloon in order to increase potential reward. At any point, participants can decide to cash-out to harvest the reward, or they can continue, risking a balloon pop that erases all earnings. We found that among seniors, increasing age was associated with greater reward-related risk taking when the balloon has a higher probability of popping (i.e., a “high risk” condition). Cognitive modeling results from hierarchical Bayesian estimation suggested that performance differences were due to increased reward sensitivity in high risk conditions in seniors.

How the aging brain translates motivational incentive into action: the role of individual differences in striato-cortical white matter pathways

The anticipation of reward enhances actions that lead to those rewards, but individuals differ in how effectively motivational incentives modulate their actions. Such individual differences are particularly prominent in aging. In order to account for such inter-individual variability among older adults, we approach the neurobiological mechanisms of motivated behavior from an individual differences perspective focusing on white matter pathways in the aging brain. Using analyses of probabilistic tractography seeded in the striatum, we report that the estimated strength of cortico-striatal and intra-striatal white matter pathways among older adults correlated with how effectively motivational incentives modulated their actions. Specifically, individual differences in the extent to which elderly participants utilized reward cues to prepare and perform more efficient antisaccades predicted structural connectivity of the striatum with cortical areas involved in reward anticipation and oculomotor control. These striatal connectivity profiles endow us with a network account for individual differences in motivated behavior among older adults. More generally, the data suggest that capturing individual differences may be crucial to better understand developmental trajectories in motivated behavior.

Error blindness and motivational significance: Shifts in networks centering on anterior insula co-vary with error awareness and pupil dilation

Abstract This investigation aims to further our understanding of the brain mechanisms underlying the awareness of one’s erroneous actions. While all errors are registered as such in the rostral cingulate zone, errors enter awareness only when the anterior insula cortex is activated. Aware but not unaware errors elicit autonomic nervous system reactivity. Our aim is to investigate the hypothesis that activation in the insula during error awareness is related to autonomic arousal and to inter‐regional interactions with other areas of the brain. To examine the role of the anterior insula in error awareness, we assessed its functional connectivity to other brain regions along with autonomic nervous system reactivity in young healthy participants who underwent simultaneous pupil‐diameter and functional magnetic resonance imaging measurements while performing a complex and error‐prone task. Error blindness was associated with failures to engage sufficient autonomic reactivity. During aware errors increased pupil‐diameter along with increased task‐related activation within, and increased connectivity between anterior insula and task‐related networks suggested an increased capacity for action‐control information transfer. Increased pupil‐diameter during aware errors was furthermore associated with decreased activation of the default‐mode network along with decreased insular connectivity with regions of the default mode system, possibly reflecting decreased task‐irrelevant information processing. This shifting mechanism may be relevant to a better understanding of how the brain and the autonomic nervous system interact to enable efficient adaptive behavior during cognitive challenge

Frontostriatal anatomical connections predict age- and difficulty-related differences in reinforcement learning.

Reinforcement learning (RL) is supported by a network of striatal and frontal cortical structures that are connected through white-matter fiber bundles. With age, the integrity of these white-matter connections declines. The role of structural frontostriatal connectivity in individual and age-related differences in RL is unclear, although local white-matter density and diffusivity have been linked to individual differences in RL. Here we show that frontostriatal tract counts in young human adults (aged 18-28), as assessed noninvasively with diffusion-weighted magnetic resonance imaging and probabilistic tractography, positively predicted individual differences in RL when learning was difficult (70% valid feedback). In older adults (aged 63-87), in contrast, learning under both easy (90% valid feedback) and difficult conditions was predicted by tract counts in the same frontostriatal network. Furthermore, network-level analyses showed a double dissociation between the task-relevant networks in young and older adults, suggesting that older adults relied on different frontostriatal networks than young adults to obtain the same task performance. These results highlight the importance of successful information integration across striatal and frontal regions during RL, especially with variable outcomes.