Feedback-related Activity Research Articles

Altered Feedback-Related Negativity in Mild Cognitive Impairment

Feedback-related negativity (FRN) is electrical brain activity related to the function of monitoring behavior and its outcome. FRN is generated by negative feedback input, such as punishment or monetary loss, and its potential is distributed maximally over the frontal-central part of the skull. Our previous study demonstrated that FRN latency was delayed and that the amplitude was increased in patients with mild Alzheimer's disease (AD). As mild cognitive impairment (MCI) is considered to be a prodromal stage of AD, we speculated that FRN would also be altered in MCI, as in AD. The aim of this study is to examine whether MCI patients showed changes in FRN during a gambling task. Thirteen MCI patients and thirteen age-matched healthy elderly individuals participated in a simple gambling task and underwent neuro-psychological assessments. The participants were asked to choose one out of two options and randomly received positive or negative feedback to their response. An EEG was recorded during the task, and FRN was obtained by subtracting the positive feedback-related activity from the negative feedback-related activity. The reaction time to probe stimuli was comparable in the two groups. The group comparisons revealed that the FRN amplitude was significantly larger for the MCI group than for the healthy elderly (F(1,24) = 6.4, ηp2 = 0.22, p = 0.019), but there was no group difference in the FRN latency. The FRN amplitude at the frontocentral electrode positively correlated with the mini-mental state examination score (Spearman's rhopartial = 0.41, p = 0.043). The finding of increased FRN amplitude in MCI was consistent with the previous finding in AD. Our findings indicate that monitoring dysfunction might also be involved in the prodromal stage of dementia.

No Evidence that Predictions and Attention Modulate the First Feedforward Sweep of Cortical Information Processing.

Predictive coding models propose that predictions (stimulus likelihood) reduce sensory signals as early as primary visual cortex (V1), and that attention (stimulus relevance) can modulate these effects. Indeed, both prediction and attention have been shown to modulate V1 activity, albeit with fMRI, which has low temporal resolution. This leaves it unclear whether these effects reflect a modulation of the first feedforward sweep of visual information processing and/or later, feedback-related activity. In two experiments, we used electroencephalography and orthogonally manipulated spatial predictions and attention to address this issue. Although clear top-down biases were found, as reflected in pre-stimulus alpha-band activity, we found no evidence for top-down effects on the earliest visual cortical processing stage (<80 ms post-stimulus), as indexed by the amplitude of the C1 event-related potential component and multivariate pattern analyses. These findings indicate that initial visual afferent activity may be impenetrable to top-down influences by spatial prediction and attention.

Dynamics of error-related activity in deterministic learning - an EEG and fMRI study

There is a close relationship between progress in learning and the error-monitoring system. EEG and fMRI studies using probabilistic learning have revealed the distinct dynamics of this system after response and feedback, i.e. an increase of error-related and a decrease of feedback-related activity in the anterior cingulate cortex (ACC). Based on the existing theories, it can be presumed that during deterministic learning feedback-related activity in ACC would also increase. Since these assumptions have not yet been confirmed, it can be only speculated based on the data from the probabilistic paradigms how the information is being integrated within the ACC during deterministic learning. Here we implemented the Paired Associate Deterministic Learning task to the EEG and fMRI experiments. The analysis of EEG data showed a significant increase in the amplitude for both ERN and FN. Similarly, the fMRI results showed an increase in response-related and feedback-related activity of the ACC in erroneous trials. Our findings are in line with the current theories of ACC function: increasing ACC activity can be linked to the detected discrepancy between expected and obtained outcomes. We argue that expectancy violations in the course of deterministic learning are signalled by both, internal and external evaluation system.

The Effects of Nicotine and Tobacco Use on Brain Reward Function: Interaction With Nicotine Dependence Severity.

This study investigated the effects of nicotine/tobacco on neural activation during performance of a monetary incentive delay task. Prior to each scan, nonsmokers received nicotine or placebo nasal spray, and smokers were smoking satiated or 24-hour withdrawn. During the scan, participants made timed responses to reward-related cues and received feedback. Parameter estimates from cue- and feedback-related activation in medial prefrontal regions and the nucleus accumbens were extracted and underwent within- and between-group analyses. Smokers' nicotine dependence severity was included as a continuous predictor variable for neural activation. Among smokers (n = 21), withdrawal decreased cue-related activation in the supplementary motor area and ventromedial prefrontal cortex, and the difference in activation (satiety > withdrawal) in these regions negatively correlated with nicotine dependence severity (Fagerström Test for Nicotine Dependence). Among nonsmokers (n = 22), nicotine increased the difference in nucleus accumbens activation between rewarded and nonrewarded feedback phases. Tobacco withdrawal and acute nicotine also had widespread effects on activation throughout the brain during the feedback phase. Acute nicotine in nonsmokers may have increased the salience of feedback information, but produced few effects on reward-related activation overall, perhaps reflecting nicotine's modest, indirect effects on reward processing. Conversely, tobacco withdrawal decreased activation compared with satiety, and this difference between conditions correlated with nicotine dependence severity. This suggests that as smokers become more dependent on nicotine, tobacco withdrawal has a more pronounced effect on reward processing. Relative to the acute effects of nicotine in nonsmokers, withdrawal from daily tobacco use had more significant effects on reward-related brain activation. This study suggests that the effects of tobacco withdrawal on reward-related brain function interact with subjects' level of nicotine dependence severity. These are potentially important sources of variability that could contribute to smoking cessation outcomes.

Fatigue Is Associated With Altered Monitoring and Preparation of Physical Effort in Patients With Chronic Fatigue Syndrome

BackgroundChronic fatigue syndrome (CFS) is characterized by disabling fatigue, which is suggested to be maintained by dysfunctional beliefs. Fatigue and its maintenance are recently conceptualized as arising from abnormally precise expectations about bodily inputs and from beliefs of diminished control over bodily states, respectively. This study used functional neuroimaging to identify the neural correlates of fatigue and its maintenance by beliefs during a physical effort task. MethodsWe isolated behavioral adjustments and cerebral activity during feedback processing and motor preparation, in the context of a task in which patients with CFS (n = 85) and healthy control subjects (n = 29) produced 30%, 50%, and 70% of their right-hand maximal voluntary contraction, and received directional feedback on performance (e.g., too little force). ResultsPatients with CSF showed an effort-dependent behavioral bias toward less effort investment in response to directional feedback for the highest effort level as compared with healthy control subjects. This bias was associated with reduced feedback-related activity in the dorsolateral prefrontal cortex. These effects were proportional to state-related fatigue and prior beliefs about CFS patients’ ability to perform the task. Patients with CFS also showed higher activity in the supplementary motor area, proportional to their state-related fatigue, and reduced connectivity between the supplementary motor area and sensorimotor cortex during motor preparation as compared with control subjects. ConclusionsThese findings link fatigue symptoms to alterations in behavioral choices on effort investment, prefrontal functioning, and supplementary motor area connectivity, with the dorsolateral prefrontal cortex being associated with prior beliefs about physical abilities.

149 Human Subthalamic Nucleus Neurons Exhibit Increased Theta-band Phase-locking During High-conflict Decision Making

Abstract INTRODUCTION The subthalamic nucleus (STN) is thought to be preferentially engaged during high-conflict decision making in humans. The population neuronal spike rate in the STN has been reported to increase during decision conflict. Conflict and feedback-related activity is also reflected in theta-band (4-8 Hz) oscillations in the STN. It remains unknown how single-neuron activity and theta-band local field potentials (LFP) oscillations interact to support decision making. METHODS We simultaneously recorded single-neuron spike activity and LFP from the STN of eight Parkinson's disease (PD) patients while they performed a novel Aversion-Reward conflict (ARC) task. Subjects decide whether to accept an offer of a monetary reward paired with a variable risk of an aversive air puff to the eye. By varying the reward and risk, we are able to study approach-avoidance decision making across a range of conflict. Using this task, we examined the mechanism of how theta-frequency oscillation and entrained single neurons involve humans' integration of cost and benefit and decision at various conflict statuses. RESULTS &gt;The ARC task reveals diverse risk-reward tradeoff strategies of patients. Consistent across patients, there is a positive correlation between the degree of decision conflict and reaction time (e.g., higher conflict offers require longer for subjects to decide). During high-conflict decisions, LFP in STN had increased activity of sub-theta oscillation, while increased activity of theta was found during low-conflict decisions. Single-trial STN theta-band power was correlated with degree of decision conflict. Interestingly, the decision to take or forgo the reward is predicted by theta-frequency phase-locked of STN neurons. CONCLUSION Our findings support the hypothesis that theta-band oscillations in single-neurons reflect the engagement of STN during conflict decision making. Furthermore, STN neurons with theta-band entrainment correlate with willingness to approach risk to pursue reward.

Probabilistic Reinforcement Learning in Patients With Schizophrenia: Relationships to Anhedonia and Avolition

Anhedonia (a reduced experience of pleasure) and avolition (a reduction in goal-directed activity) are common features of schizophrenia that have substantial effects on functional outcome, but are poorly understood and treated. Here, we examined whether alterations in reinforcement learning may contribute to these symptoms in schizophrenia by impairing the translation of reward information into goal-directed action. 38 stable outpatients with schizophrenia or schizoaffective disorder and 37 healthy controls underwent fMRI during a probabilistic stimulus selection reinforcement learning task with dissociated choice- and feedback-related activation, followed by a behavioral transfer task allowing separate assessment of learning from positive versus negative outcomes. A Q-learning algorithm was used to examine functional activation relating to prediction error at the time of feedback and to expected value at the time of choice. Behavioral results suggested a reduction in learning from positive feedback in patients; however, this reduction was unrelated to anhedonia/avolition severity. On fMRI analysis, prediction error-related activation at the time of feedback was highly similar between patients and controls. During early learning, patients activated regions in the cognitive control network to a lesser extent than controls. Correlation analyses revealed reduced responses to positive feedback in dorsolateral prefrontal cortex and caudate among those patients higher in anhedonia/avolition. Together, these results suggest that anhedonia/avolition are as strongly related to cortical learning or higher-level processes involved in goal-directed behavior such as effort computation and planning as to striatally mediated learning mechanisms.

How to be patient. The ability to wait for a reward depends on menstrual cycle phase and feedback-related activity.

Dopamine (DA) plays a major role in reinforcement learning with increases promoting reward sensitivity (Go learning) while decreases facilitate the avoidance of negative outcomes (NoGo learning). This is also reflected in adaptations of response time: higher levels of DA enhance speeding up to get a reward, whereas lower levels favor slowing down. The steroid hormones estradiol and progesterone have been shown to modulate dopaminergic tone. Here, we tested 14 women twice during their menstrual cycle, during the follicular (FP) and the luteal phase (LP), applying functional magnetic resonance imaging while they performed a feedback learning task. Subsequent behavioral testing assessed response time preferences with a clock task, in which subjects had to explore the optimal response time (RT) to maximize reward. In the FP subjects displayed a greater learning-related change of their RT than during the LP, when they were required to slow down. Final RTs in the slow condition were also predicted by feedback-related brain activation, but only in the FP. Increased activation of the inferior frontal junction and rostral cingulate zone was thereby predictive of slower and thus better adapted final RTs. Conversely, final RT was faster and less optimal for reward maximization if activation in the ventromedial prefrontal cortex was enhanced. These findings show that hormonal shifts across the menstrual cycle affect adaptation of response speed during reward acquisition with higher RT adjustment in the FP in the condition that requires slowing down. Since high estradiol levels during the FP increase synaptic DA levels, this conforms well to our hypothesis that estradiol supports Go learning at the expense of NoGo learning. Brain-behavior correlations further indicated that the compensatory capacity to counteract the follicular Go bias may be linked to the ability to more effectively monitor action outcomes and suppress bottom-up reward desiring during feedback processing.

Midcingulate Motor Map and Feedback Detection: Converging Data from Humans and Monkeys.

The functional and anatomical organization of the cingulate cortex across primate species is the subject of considerable and often confusing debate. The functions attributed to the midcingulate cortex (MCC) embrace, among others, feedback processing, pain, salience, action-reward association, premotor functions, and conflict monitoring. This multiplicity of functional concepts suggests either unresolved separation of functional contributions or integration and convergence. We here provide evidence from recent experiments in humans and from a meta-analysis of monkey data that MCC feedback-related activity is generated in the rostral cingulate premotor area by specific body maps directly related to the modality of feedback. As such, we argue for an embodied mechanism for adaptation and exploration in MCC. We propose arguments and precise tools to resolve the origins of performance monitoring signals in the medial frontal cortex, and to progress on issues regarding homology between human and nonhuman primate cingulate cortex.

Effects of social context on feedback-related activity in the human ventral striatum

It is now well established that activation of the ventral striatum (VS) encodes feedback related information, in particular, aspects of feedback validity, reward magnitude, and reward probability. More recent findings also point toward a role of VS in encoding social context of feedback processing. Here, we investigated the effect of social observation on neural correlates of feedback processing. To this end, subjects performed a time estimation task and received positive, negative, or uninformative feedback. In one half of the experiment subjects thought that an experimenter closely monitored their face via a camera. We successfully replicated an elevated VS response to positive relative to negative feedback. Further, our data demonstrate that this reward-related activation of the VS is increased during observation by others. Using uninformative feedback as reference condition, we show that specifically VS activation during positive feedback was modulated by observation manipulation. Our findings support accounts which posit a role of VS in integrating social context into the processing of feedback and, in doing so, signaling its social relevance.

The Location of Feedback-Related Activity in the Midcingulate Cortex Is Predicted by Local Morphology

Information processing in the medial frontal cortex is often said to be modulated in pathological conditions or by individual traits. This has been observed in neuroimaging and event-related potential studies centered in particular on midcingulate cortex (MCC) functions. This region of the brain is characterized by considerable intersubject morphological variability. Whereas in a subset of hemispheres only a single cingulate sulcus (cgs) is present, a majority of hemispheres exhibit an additional sulcus referred to as the paracingulate sulcus (pcgs). The present functional magnetic resonance imaging study defined the relationship between the local morphology of the cingulate/paracingulate sulcal complex and feedback-related activity. Human subjects performed a trial-and-error learning task in which they had to discover which one of a set of abstract stimuli was the best option. Feedback was provided by means of fruit juice, as in studies with monkeys. A subject-by-subject analysis revealed that the feedback-related activity during exploration was systematically located in the cgs when no pcgs was observed, but in the pcgs when the latter sulcus was present. The activations had the same functional signature when located in either the cgs or in the pcgs, confirming that both regions were homologues. Together, the results show that the location of feedback-related MCC activity can be predicted from morphological features of the cingulate/paracingulate complex.

Factors mediating performance monitoring in humans—from context to personality

Factors mediating performance monitoring in humans—from context to personality

The Time Course of Segmentation and Cue-Selectivity in the Human Visual Cortex

Texture discontinuities are a fundamental cue by which the visual system segments objects from their background. The neural mechanisms supporting texture-based segmentation are therefore critical to visual perception and cognition. In the present experiment we employ an EEG source-imaging approach in order to study the time course of texture-based segmentation in the human brain. Visual Evoked Potentials were recorded to four types of stimuli in which periodic temporal modulation of a central 3° figure region could either support figure-ground segmentation, or have identical local texture modulations but not produce changes in global image segmentation. The image discontinuities were defined either by orientation or phase differences across image regions. Evoked responses to these four stimuli were analyzed both at the scalp and on the cortical surface in retinotopic and functional regions-of-interest (ROIs) defined separately using fMRI on a subject-by-subject basis. Texture segmentation (tsVEP: segmenting versus non-segmenting) and cue-specific (csVEP: orientation versus phase) responses exhibited distinctive patterns of activity. Alternations between uniform and segmented images produced highly asymmetric responses that were larger after transitions from the uniform to the segmented state. Texture modulations that signaled the appearance of a figure evoked a pattern of increased activity starting at ∼143 ms that was larger in V1 and LOC ROIs, relative to identical modulations that didn't signal figure-ground segmentation. This segmentation-related activity occurred after an initial response phase that did not depend on the global segmentation structure of the image. The two cue types evoked similar tsVEPs up to 230 ms when they differed in the V4 and LOC ROIs. The evolution of the response proceeded largely in the feed-forward direction, with only weak evidence for feedback-related activity.

An fMRI study of risk‐taking following wins and losses: Implications for the gambler's fallacy

Human decision-making involving independent events is often biased and affected by prior outcomes. Using a controlled task that allows us to manipulate prior outcomes, the present study examined the effect of prior outcomes on subsequent decisions in a group of young adults. We found that participants were more risk-seeking after losing a gamble (riskloss) than after winning a gamble (riskwin), a pattern resembling the gambler's fallacy. Functional MRI data revealed that decisions after riskloss were associated with increased activation in the frontoparietal network, but decreased activation in the caudate and ventral striatum. The increased risk-seeking behavior after a loss showed a trend of positive correlation with activation in the frontoparietal network and the left lateral orbitofrontal cortex but a trend of negative correlation with activation in the amgydala and caudate. In addition, there was a trend of positive correlation between feedback-related activation in the left lateral frontal cortex and subsequent increased risk-seeking behavior. These results suggest that a strong cognitive control mechanism but a weak affective decision-making and reinforcement learning mechanism that usually contribute to flexible, goal-directed decisions can lead to decision biases involving random events. This has significant implications for our understanding of the gambler's fallacy and human decision making under risk.

Dissociation of response and feedback negativity in schizophrenia: electrophysiological and computational evidence for a deficit in the representation of value.

Contrasting theories of schizophrenia propose that the disorder is characterized by a deficit in phasic changes in dopamine activity in response to ongoing events or, alternatively, by a weakness in the representation of the value of responses. Schizophrenia patients have reliably reduced brain activity following incorrect responses but other research suggests that they may have intact feedback-related potentials, indicating that the impairment may be specifically response-related. We used event-related brain potentials and computational modeling to examine this issue by comparing the neural response to outcomes with the neural response to behaviors that predict outcomes in patients with schizophrenia and psychiatrically healthy comparison subjects. We recorded feedback-related activity in a passive gambling task and a time estimation task and error-related activity in a flanker task. Patients’ brain activity following an erroneous response was reduced compared to comparison subjects but feedback-related activity did not differ between groups. To test hypotheses about the possible causes of this pattern of results, we used computational modeling of the electrophysiological data to simulate the effects of an overall reduction in patients’ sensitivity to feedback, selective insensitivity to positive or negative feedback, reduced learning rate, and a decreased representation of the value of the response given the stimulus on each trial. The results of the computational modeling suggest that schizophrenia patients exhibit weakened representation of response values, possibly due to failure of the basal ganglia to strongly associate stimuli with appropriate response alternatives.

Genetic influences on feedback-related neural activity in a gambling task

Genetic influences on feedback-related neural activity in a gambling task

Neuroelectric Signatures of Reward Learning and Decision-Making in the Human Nucleus Accumbens

Learning that certain actions lead to risky rewards is critical for biological, social, and economic survival, but the precise neural mechanisms of such reward-guided learning remain unclear. Here, we show that the human nucleus accumbens plays a key role in learning about risks by representing reward value. We recorded electrophysiological activity directly from the nucleus accumbens of five patients undergoing deep brain stimulation for treatment of refractory major depression. Patients engaged in a simple reward-learning task in which they first learned stimulus-outcome associations (learning task), and then were able to choose from among the learned stimuli (choosing task). During the learning task, nucleus accumbens activity reflected potential and received reward values both during the cue stimulus and during the feedback. During the choosing task, there was no nucleus accumbens activity during the cue stimulus, but feedback-related activity was pronounced and similar to that during the learning task. This pattern of results is inconsistent with a prediction error response. Finally, analyses of cross-correlations between the accumbens and simultaneous recordings of medial frontal cortex suggest a dynamic interaction between these structures. The high spatial and temporal resolution of these recordings provides novel insights into the timing of activity in the human nucleus accumbens, its functions during reward-guided learning and decision-making, and its interactions with medial frontal cortex.

Learn from Your Mistakes

Human experience is based on learning that our actions affect subsequent positive or negative outcomes. Rewards strengthen associations between contextual stimuli and actions, thereby reinforcing and maintaining successful behavior, whereas punishments induce avoidance of erroneous actions. While we usually learn from both positive and negative reinforcement, the relative amount of learning from success or errors varies between individuals. Klein et al . investigated a human genetic polymorphism associated with the density of brain dopamine D2 receptor. Reduced D2 receptor density was associated with less-efficient learning from errors. In people with lower D2 receptor density, the reduced capacity to learn from errors was accompanied by reduced feedback-related activity in the posterior medial frontal cortex, an area known to monitor for negative action outcomes. T. A. Klein, J. Neumann, M. Reuter, J. Hennig, D. Y. von Cramon, M. Ullsperger, Genetically determined differences in learning from errors. Science 318 , 1642-1645 (2007). [Abstract] [Full Text]

Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents

Adolescents' propensity for risk-taking and reward-seeking behaviors suggests a heightened sensitivity for reward, reflected by greater feedback-related activity changes in reward circuitry (e.g., nucleus accumbens), and/or a lower sensitivity to potential harm reflected by weaker feedback-related activity changes in avoidance circuitry (e.g., amygdala) relative to adults. Responses of nucleus accumbens and amygdala to valenced outcomes (reward receipt and reward omission) were assayed using an event-related functional magnetic resonance imaging procedure paired with a monetary reward task in 14 adults and 16 adolescents. Bilateral amygdala and nucleus accumbens showed significantly greater activation when winning than when failing to win in both groups. Group comparisons revealed stronger activation of left nucleus accumbens by adolescents, and of left amygdala by adults. When examining responses to reward receipts and to reward omissions separately, the most robust group difference was within the amygdala during reward omission. The reduction of the fMRI BOLD signal in the amygdala in response to reward omission was larger for adults than for adolescents. Correlations showed a close link between negative emotion and amygdala decreased BOLD signal in adults, and between positive emotion and nucleus accumbens activation in adolescents. Overall, these findings support the notion that the signal differences between positive and negative outcomes involve the nucleus accumbens more in adolescents than in adults, and the amygdala more in adults than in adolescents. These developmental differences, if replicated, may have important implications for the development of early-onset disorders of emotion and motivation.

Dissociable concurrent activity of lateral and medial frontal lobe during negative feedback processing

External feedback on results of one's behavior guides flexible adaptation to changing environments. It has been suggested that the lateral and medial parts of the frontal lobe are responsible for cognitive and emotional functions, respectively. In the present fMRI study, multiple mental components evoked by the presentation of negative feedback were dissociated along the cognitive–emotional axis in set-shifting paradigms. The double dissociation of the concurrent feedback-related activity was observed in the right frontal lobe: the lateral frontal lobe was associated with the inferential component, whereas the medial frontal lobe was associated with the emotional component. However, among the multiple right lateral frontal regions, a region of interest (ROI) analysis indicated that the inferential component was not dominant in the region near the inferior frontal junction. The medial frontal activations were observed ventral and anterior to the presupplementary motor area, and dorsal and posterior to the anterior cingulate cortex. The double dissociation in the right frontal lobe suggests that the lateral and medial frontal lobe cooperatively but differentially contributes to the negative feedback processing, demonstrating the lateral–medial dichotomy of the frontal lobe functions suggested by previous neuropsychological studies. At the same time, the functional heterogeneity in the lateral and medial frontal lobe demands modifications of the traditional view of the functional organization of the frontal lobe.