Neural responses to negative feedback are related to negative emotionality in healthy adults

Prior neuroimaging and electrophysiological evidence suggests that potentiated responses in the anterior cingulate cortex (ACC), particularly the rostral ACC, may contribute to abnormal responses to negative feedback in individuals with elevated negative affect and depressive symptoms. The feedback-related negativity (FRN) represents an electrophysiological index of ACC-related activation in response to performance feedback. The purpose of the present study was to examine the FRN and underlying ACC activation using low resolution electromagnetic tomography source estimation techniques in relation to negative emotionality (a composite index including negative affect and subclinical depressive symptoms). To this end, 29 healthy adults performed a monetary incentive delay task while 128-channel event-related potentials were recorded. We found that enhanced FRNs and increased rostral ACC activation in response to negative-but not positive-feedback was related to greater negative emotionality. These results indicate that individual differences in negative emotionality-a putative risk factor for emotional disorders-modulate ACC-related processes critically implicated in assessing the motivational impact and/or salience of environmental feedback.     

The feedback-related negativity is modulated by feedback probability in observational learning

The feedback-related negativity (FRN), an event-related potentials (ERPs) component reflecting activity of the anterior cingulate cortex (ACC), has been shown to be modulated by feedback expectancy following active choices in feedback-based learning tasks. A general reduction of FRN amplitude has been described in observational feedback learning, raising the question whether FRN amplitude is modulated in a similar way in this type of learning. The present study investigated whether the FRN and the P300 - a second ERP component related to feedback processing - are modulated by feedback probability in observational learning. Thirty-two subjects participated in the experiment. They observed a virtual person choosing between two symbols and receiving positive or negative feedback. Learning about stimulus-specific feedback probabilities was assessed in active test trials without feedback. In addition, the bias to learn from positive or negative feedback and - in a subsample of 17 subjects - empathy scores were obtained. General FRN and P300 modulations by feedback probability were found across all subjects. Only for the FRN in learners, an interaction between probability and valence was observed. Larger FRN amplitudes for negative relative to positive feedback only emerged for the lowest outcome probability. The results show that feedback expectancy modulates FRN amplitude also in observational learning, suggesting a similar ACC function as in active learning. On the other hand, the modulation is only seen for very low feedback expectancy, which suggests that brain regions other than those of the reward system contribute to feedback processing in an observation setting.     

Mediofrontal negativities in the absence of responding

The feedback-related negativity (FRN) is an event-related brain potential component that is elicited by feedback stimuli indicating unfavorable outcomes. Until recently, the FRN has been studied primarily using experimental paradigms in which outcomes appeared to be contingent upon the participants' behavior. The present study further addressed the question whether an FRN can be elicited by outcomes that are not contingent on any preceding choice or action. Participants took part in a simple slot-machine task in which they experienced monetary gains and losses in the absence of responses. In addition, they performed a time estimation task often used to study the FRN and a flanker task known to elicit the error-related negativity. Outcomes in the slot-machine task elicited an FRN-like mediofrontal negativity whose amplitude correlated with the amplitude of the FRN associated with negative feedback in the time estimation task. However, the mediofrontal negativity was observed both for (unfavorable) outcomes that averted a gain and for (favorable) outcomes that averted a loss of money. The results are discussed in the framework of current conceptions of the FRN and related electrophysiological components.     

Brain potentials associated with outcome expectation and outcome evaluation

Feedback-related negativity is a negative deflection in brain potentials associated with feedback indicating monetary losses or response errors. Feedback-related negativity is studied primarily in paradigms in which participants experience negative outcomes that appear to be contingent upon their previous choices. This study investigated whether feedback-related negativity can be elicited by a randomly assigned cue indicating potential monetary loss. The expected loss or win can be materialized or averted depending on participants' performance in a subsequent game. Compared with the win cue, the loss cue elicited a weak but significant feedback-related negativity-like effect. It is suggested that the anterior cingulate cortex, which generates feedback-related negativity, may function as a pre-warning system that alerts the brain to get ready for future events.     

Detecting perceptual conflict by the feedback-related negativity in brain potentials

The feedback-related negativity (FRN) in brain potentials is typically observed for the outcome evaluation concerning one's performance or monetary reward. Using a task in which the participant guesses whether the first stimulus (S1) would have the same color as the subsequently presented second stimulus (S2), this study demonstrates that the FRN to S2, which serves as feedback to the guessing, is also sensitive to the conflict between perceptual representations of S1 and S2 in working memory. The FRN effect for the feedback concerning the correctness of one's performance is modulated by the congruency between perceptual properties of the stimuli. The anterior cingulate cortex, which generates the FRN, is thus a general conflict-monitoring device detecting both response and perceptual conflicts.     

Color Stroop and negative priming in schizophrenia: An fMRI study

Disturbances in selective attention represent a core characteristic of schizophrenia, whose neural underpinnings have yet to be fully elucidated. Consequently, we recorded brain activation using functional magnetic resonance imaging (fMRI) while 15 patients with schizophrenia and 15 age-matched controls performed a well-established measure of selective attention—the color Stroop negative priming task. We focused on two aspects of performance: overriding pre-potent responses (Stroop effect) and inhibition of prior negatively primed trials (negative priming effect). Behaviorally, controls demonstrated both significant Stroop and negative priming effects, while schizophrenic subjects only showed the Stroop effect. For the Stroop effect, fMRI indicated significantly greater activation in frontal regions–medial frontal gyrus/anterior cingulate gyrus and middle frontal gyrus for controls–but greater activation in medial parietal regions (posterior cingulate gyrus/precuneus) for patients. Negative priming elicited significant activation in right dorsolateral prefrontal cortex for both groups, but also in left dorsolateral prefrontal cortex for patients. These different patterns of fMRI activation may reflect faulty interaction in schizophrenia within networks of brain regions that are vital to selective attention.     

It is less than you expected: The feedback-related negativity reflects violations of reward magnitude expectations

The anterior cingulate cortex (ACC) is involved in performance monitoring and in learning from performance feedback. Recent research suggests that the feedback-related negativity (FRN), an event-related potentials (ERP) component reflecting neural activity in the ACC, codes the size of a negative prediction error when reward probabilities are varied. There is as yet no clear evidence that the FRN is also sensitive to violations of reward magnitude expectations. In the present study, 20 healthy young subjects engaged in a learning task in which a coin had to be found on each trial. The value of the coin (the potential reward magnitude) was varied from trial to trial and amounted to 5 cent, 20 cent or 50 cent. Analysis of ERPs revealed that FRN amplitude differences between reward and non-reward were significantly modulated by (potential) reward magnitude. This effect was driven by the neural response to non-reward: the larger the potential reward, the larger was the FRN amplitude in response to non-reward. In contrast, the P300 was larger for positive outcomes and showed an effect of (potential) reward magnitude independent of valence. Together with evidence from previous studies, these results show that the FRN codes negative prediction errors in the context of varying reward probabilities and magnitudes. The findings are in line with recent results based on functional neuroimaging and lend further support to the idea of a key role of the ACC in the integration of information on different aspects of performance outcomes.     

Reward context sensitivity impairment following severe TBI: an event-related potential investigation.

Many rehabilitation protocols following traumatic brain injury (TBI) utilize reinforcement and reward to influence behavior and facilitate recovery; however, previous studies suggest survivors of severe TBI demonstrate impairments in contingency utilization and sensitivity. The precise neurobiological mechanisms underlying these deficits have not been thoroughly explored, but can be examined using the "feedback-related negativity" (FRN)--an event-related potential (ERP) component evoked following performance or response feedback (e.g., whether a monetary reward is obtained) with a larger FRN following unfavorable than favorable outcomes--particularly when unfavorable feedback occurs in the context of high reward probability. We examined ERPs elicited by favorable (monetary gain: "reward") and unfavorable (no monetary gain: "non-reward") feedback during a guessing task where probability of reward outcome was manipulated in survivors of severe TBI and demographically matched healthy participants. Consistent with previous findings, controls showed larger amplitude FRN to non-reward feedback and the largest amplitude FRN following a non-reward when reward probability context was greatest. In contrast, FRN in TBI participants did not significantly differentiate non-reward from reward trials and their FRN was largest to reward trials in the low reward probability context. Findings implicate an electrophysiological marker of impaired reward context sensitivity following severe TBI.     

Self-relevant criteria determine the evaluation of outcomes induced by others

The evaluation of whether an outcome is good or bad is reflected in feedback-related negativity (FRN), which is an event-related brain potential (ERP) component that is elicited by bad events. It is still, however, unclear how the FRN reflects the evaluation of outcomes induced by others. We focused on the relationship between self and other, and recorded ERPs during an alternative gambling task performed by two players (participant and virtual player). FRN was elicited not only by the losses of another in a cooperative situation but also by the gains of another in an antagonistic situation. These results indicate that FRN reflects the evaluation on the basis of one's own evaluative criteria, regardless of the monetary outcome for another.     

Coupling electrophysiological and hemodynamic responses to errors

Performance errors are associated with distinct electrophysiological and hemodynamic signatures: a fronto-central error-related negativity (ERN) is seen in the event-related potentials and a network of activations including medio-frontal, parietal, and insular cortex is revealed by functional magnetic resonance imaging. We used simultaneous electroencephalography and functional magnetic resonance imaging (fMRI) to characterize the relationship between the electrophysiological and hemodynamic responses to errors. Participants performed a modified Flanker task. When analyzed independently, we found the ERN and hemodynamic activations in dorsal anterior cingulate cortex, superior frontal gyrus, precentral gyrus, inferior frontal gyrus, and inferior parietal lobule. fMRI-informed dipole modeling and joint independent component analysis (ICA) were used to couple electrophysiological and hemodynamic data. Both techniques revealed a temporal evolution of the areas found in the fMRI analysis, with the right hemisphere activations peaking before the left hemisphere. However, joint ICA added information, revealing a number of cortical and subcortical areas that had not been shown with parametric mapping. This technique also uncovered how these areas evolve over time. All together, these analyses provide a more detailed picture of the spatiotemporal dynamics of the processing of performance errors.     

Functional magnetic resonance imaging of brain activity in the visual oddball task

Abnormalities in the P300 ERP, elicited by the oddball task and measured using EEG, have been found in a number of central nervous system disorders including schizophrenia, Alzheimer's disease, and alcohol dependence. While electrophysiological studies provide high temporal resolution, localizing the P300 deficit has been particularly difficult because the measurements are collected from the scalp. Knowing which brain regions are involved in this process would elucidate the behavioral correlates of P300. The aim of this study was to determine the brain regions involved in a visual oddball task using fMRI. In this study, functional and high-resolution anatomical MR images were collected from seven normal volunteers. The data were analyzed using a randomization-based statistical method that accounts for multiple comparisons, requires no assumptions about the noise structure of the data, and does not require spatial or temporal smoothing. Activations were detected (P<0.01) bilaterally in the supramarginal gyrus (SMG; BA 40), superior parietal lobule (BA 7), the posterior cingulate gyrus, thalamus, inferior occipitotemporal cortex (BA 19/37), insula, dorsolateral prefrontal cortex (BA 9), anterior cingulate cortex (ACC), medial frontal gyrus (BA 6), premotor area, and cuneus (BA 17). Our results are consistent with previous studies that have observed activation in ACC and SMG. Activation of thalamus, insula, and the occipitotemporal cortex has been reported less consistently. The present study lends further support to the involvement of these structures in visual target detection.     

The cortical generators of P3a and P3b: a LORETA study

The P3 is probably the most well known component of the brain event-related potentials (ERPs). Using a three-tone oddball paradigm two different components can be identified: the P3b elicited by rare target stimuli and the P3a elicited by the presentation of rare non-target stimuli. Although the two components may partially overlap in time and space, they have a different scalp topography suggesting different neural generators. The present study is aimed at defining the scalp topography of the two P3 components by means of reference-independent methods and identifying their electrical cortical generators by using the low-resolution electromagnetic tomography (LORETA). ERPs were recorded during a three-tone oddball task in 32 healthy, right-handed university students. The scalp topography of the P3 components was assessed by means of the brain electrical microstates technique and their cortical sources were evaluated by LORETA. P3a and P3b showed different scalp topography and cortical sources. The P3a electrical field had a more anterior distribution as compared to the P3b and its generators were localized in cingulate, frontal and right parietal areas. P3b sources included bilateral frontal, parietal, limbic, cingulate and temporo-occipital regions. Differences in scalp topography and cortical sources suggest that the two components reflect different neural processes. Our findings on cortical generators are in line with the hypothesis that P3a reflects the automatic allocation of attention, while P3b is related to the effortful processing of task-relevant events.     

Event-related components of the punishment and reward sensitivity

ObjectiveThe present study investigated the properties of feedback-related negativity (FRN) and P3 component of the event-related potentials (ERPs) and their neural sources localization as neurocognitive correlates of the behavioural inhibition and behavioural activation systems (BIS/BAS). The association between BIS/BAS function and anterior cortical asymmetry was tested.MethodsFifty right-handed women were investigated with 30-channel recordings during an instrumental Go/No-Go learning task. ERPs were elicited to feedback signals indicating monetary losses and monetary gains. Learning performance, FRN, and P3 amplitude and latency measures were calculated and related to BIS and BAS measures by means of ANOVA and correlation analysis. The neural sources of FRN and P3 components of the ERPs were estimated using LORETA software. A resting EEG-alpha-power (8–13 Hz) asymmetry measure was obtained.ResultsHigh levels of Reward Responsiveness (RR), a first order factor of the BAS, were associated with shorter RTs and enhanced positive feelings. The FRN was larger to signals indicating monetary Loss as compared to monetary Gain and enhanced with higher BIS and individual learning ability. Higher RR scores were related to greater left-sided resting frontal cortical asymmetry associated with approach orientation. High-RR subjects, as compared to Low-RR ones, had a smaller P3 amplitude for Go/Loss signals. The P3 latency to No-Go/Gain signals was the best positive predictor of RR. LORETA source localization for the FRN component displayed significantly higher brain electrical activity in left-fusiform gyrus and right superior temporal gyrus to monetary Loss in comparison to monetary Gain after incorrect No-Go responses. For the P3 wave, the monetary Loss produced significantly higher activations in the left superior parietal lobule, right postcentral gyrus, and in the ACC.ConclusionThe FRN was sensitive to cues of punishment and higher BIS was uniquely related to a larger FRN amplitude on No-Go/Loss trials, linking BIS with conflict monitoring and sensitivity to No-Go cues. Furthermore, the significant interaction found between BIS and RR on FRN amplitude together with the findings linking High-RR levels with shorter RTs, smaller P3 amplitudes and enhanced positive feelings are in line with the hypothesis that both BIS and BAS have the potential to influence punishment-mediated and reward-mediated behaviour.SignificanceResults open up new perspectives for future investigations on the relationship between BIS/BAS measures and ERP components to monetary reward during learning.     

Abnormal baseline brain activity in low-grade hepatic encephalopathy: a resting-state fMRI study

Resting-state functional magnetic resonance imaging (fMRI) has been used to detect the alterations of spontaneous neuronal activity in various neuropsychiatric diseases, but rarely in low-grade hepatic encephalopathy (HE), a common neuropsychiatric complication of liver cirrhosis. We conducted a resting-state fMRI in 19 healthy controls, 18 cirrhotic patients without HE, and 22 cirrhotic patients with low-grade HE. The amplitude of low-frequency fluctuations (ALFF) of fMRI signal was computed to measure the spontaneous neuronal activity. Several regions showing significant ALFF differences among three groups were the precuneus, occipital lobe, left frontal lobe and anterior/middle cingulate cortex, and left cerebellum posterior lobe. Compared to controls or patients without HE, patients with low-grade HE showed decreased ALFF in the precuneus and adjacent cuneus, visual cortex, and left cerebellum posterior lobe. Compared to controls, patients with low-grade HE showed higher ALFF in both cortical and subcortical regions, including the right middle cingulate gyrus, and left anterior/middle cingulate gyrus, inferior frontal gyrus, insula lobe, parahippocampal gyrus, middle temporal gyrus and lentiform nucleus; compared to patients without HE, patients with low-grade HE showed higher ALFF in the left medial frontal gyrus and anterior cingulate gyrus, bilateral superior frontal gyrus, and right middle frontal gyrus. Moreover, correlations between ALFF changes and poor neurocognitive performances were found in patients with low-grade HE. These results suggested the existence of aberrant brain activity at the baseline state in low-grade HE, which may be implicated in the neurological pathophysiology underlying HE.     

Neural correlates of episodic and semantic memory retrieval in borderline personality disorder: An fMRI study

Verbal memory impairment in borderline personality disorder (BPD) is still a matter of debate. In this study we combine investigations of both, memory retrieval as well as underlying neural circuits in BPD. Functional magnetic resonance imaging (fMRI) was used to study regional brain activation in 18 right-handed female patients with BPD and 18 matched controls during the retrieval of an episodic memory retrieval (EMR) task (free recall of a word list) and a semantic memory retrieval (SMR) task (verbal fluency). Despite unaffected performance in EMR and SMR, patients with BPD showed task-specific increased activation compared with controls. During EMR, the increased activation encompassed the posterior cingulate cortex bilaterally, the left middle and superior temporal gyrus, the right inferior frontal gyrus, and the right angular gyrus. SMR was associated with increased activation of the posterior cingulate cortex, of the right fusiform gyrus, of the left anterior cingulate cortex, and of the left postcentral gyrus. Our findings suggest that BPD patients may need to engage larger brain areas to reach a level of performance in episodic and semantic retrieval tasks that is comparable to that of healthy controls.     

The processing of unexpected positive response outcomes in the mediofrontal cortex

The human mediofrontal cortex, especially the anterior cingulate cortex, is commonly assumed to contribute to higher cognitive functions like performance monitoring. How exactly this is achieved is currently the subject of lively debate but there is evidence that an event's valence and its expectancy play important roles. One prominent theory, the reinforcement learning theory by Holroyd and colleagues (2002, 2008), assigns a special role to feedback valence, while the prediction of response-outcome (PRO) model by Alexander and Brown (2010, 2011) claims that the mediofrontal cortex is sensitive to unexpected events regardless of their valence. However, paradigms examining this issue have included confounds that fail to separate valence and expectancy. In the present study, we tested the two competing theories of performance monitoring by using an experimental task that separates valence and unexpectedness of performance feedback. The feedback-related negativity of the event-related potential, which is commonly assumed to be a reflection of mediofrontal cortex activity, was elicited not only by unexpected negative feedback, but also by unexpected positive feedback. This implies that the mediofrontal cortex is sensitive to the unexpectedness of events in general rather than their valence and by this supports the PRO model.     

Attention orienting dysfunction during salient novel stimulus processing in schizophrenia

Schizophrenia is characterised by marked disturbances of attention and information processing. Patients experience difficulty focusing on relevant cues and avoiding distraction by irrelevant stimuli. Event-related potential recordings indicate an amplitude reduction in the P3a component elicited by involuntary orienting to task-irrelevant, infrequent novel stimuli presented during auditory oddball detection in patients with schizophrenia. The goal of the present study was to elucidate the functional abnormality underlying the disturbed orienting to novel stimuli in schizophrenia. Twenty-eight stable, partially remitted, medicated patients with schizophrenia and 28 healthy control participants completed a novelty oddball variant during event-related fMRI. Relative to healthy participants, patients with schizophrenia were characterised by underactivity during novel stimulus processing in the right amygdala-hippocampus, within paralimbic cortex in the rostral anterior cingulate and posterior cingulate cortices and the right frontal operculum, and in association cortex at the right temporo-parietal-occipital junction, bilateral intraparietal sulcus, and bilateral dorsal frontal cortex. Subcortically, relative hypoactivation during novelty processing was apparent in the cerebellum, thalamus, and basal ganglia. These results suggest that patients less efficiently reorient processing resources away from the ongoing task of detecting and responding to the task-relevant target stimuli. In addition, trend results suggest that patients experienced increased distraction by novel stimuli.     

Learning-related changes in reward expectancy are reflected in the feedback-related negativity

The feedback-related negativity (FRN) has been hypothesized to be linked to reward-based learning. While many studies have shown that the FRN only occurs in response to unexpected negative outcomes, the relationship between the magnitude of negative prediction errors and FRN amplitude remains a matter of debate. The present study aimed to elucidate this relationship with a new behavioural procedure that allowed subjects to predict precise reward probabilities by learning an explicit rule. Insight into the rule did not only influence subjects' choice behaviour, but also outcome-related event-related potentials. After subjects had learned the rule, the FRN amplitude difference between non-reward and reward mirrored the magnitude of the negative prediction error, i.e. it was larger for less likely negative outcomes. Source analysis linked this effect to the anterior cingulate cortex. P300 amplitude was also modulated by outcome valence and expectancy. It was larger for positive and unexpected outcomes. It remains to be clarified, however, whether the P300 reflects a positive prediction error.     

Temporal dynamics of reward processing revealed by magnetoencephalography

Monetary gains and losses in gambling situations are associated with a distinct electroencephalographic signature: in the event-related potentials (ERPs), a mediofrontal feedback-related negativity (FRN) is seen for losses, whereas oscillatory activity shows a burst of in the θ-range for losses and in the β-range for gains. We used whole-head magnetoencephalography to pinpoint the magnetic counterparts of these effects in young healthy adults and explore their evolution over time. On each trial, participants bet on one of two visually presented numbers (25 or 5) by button-press. Both numbers changed color: if the chosen number turned green (red), it indicated a gain (loss) of the corresponding sum in Euro cent. For losses, we found the magnetic correlate of the FRN extending between 230 and 465 ms. Source localization with low-resolution electromagnetic tomography indicated a first generator in posterior cingulate cortex with subsequent activity in the anterior cingulate cortex. Importantly, this effect was sensitive to the magnitude of the monetary loss (25 cent > 5 cent). Later activation was also found in the right insula. Time-frequency analysis revealed a number of oscillatory components in the theta, alpha, and high-beta/low-gamma bands associated to gains, and in the high-beta band, associated to the magnitude of the loss. All together, these effects provide a more fine-grained picture of the temporal dynamics of the processing of monetary rewards and losses in the brain.     

Error-related brain activation during a Go/NoGo response inhibition task

Inhibitory control and performance monitoring are critical executive functions of the human brain. Lesion and imaging studies have shown that the inferior frontal cortex plays an important role in inhibition of inappropriate response. In contrast, specific brain areas involved in error processing and their relation to those implicated in inhibitory control processes are unknown. In this study, we used a random effects model to investigate error-related brain activity associated with failure to inhibit response during a Go/NoGo task. Error-related brain activation was observed in the rostral aspect of the right anterior cingulate (BA 24/32) and adjoining medial prefrontal cortex, the left and right insular cortex and adjoining frontal operculum (BA 47) and left precuneus/posterior cingulate (BA 7/31/29). Brain activation related to response inhibition and competition was observed bilaterally in the dorsolateral prefrontal cortex (BA 9/46), pars triangularis region of the inferior frontal cortex (BA 45/47), premotor cortex (BA 6), inferior parietal lobule (BA 39), lingual gyrus and the caudate, as well as in the right dorsal anterior cingulate cortex (BA 24). These findings provide evidence for a distributed error processing system in the human brain that overlaps partially, but not completely, with brain regions involved in response inhibition and competition. In particular, the rostal anterior cingulate and posterior cingulate/precuneus as well as the left and right anterior insular cortex were activated only during error processing, but not during response competition, inhibition, selection, or execution. Our results also suggest that the brain regions involved in the error processing system overlap with brain areas implicated in the formulation and execution of articulatory plans.