My choice, my actions: self-determination, not instrumental value of outcomes enhances outcome monitoring during learning.

Freedom of choice enhances our sense of agency. During goal-directed behavior, the freedom to choose between different response options increases the neural processing of positive and negative feedback, indicating enhanced outcome monitoring under conditions of high agency experience. However, it is unclear whether this enhancement is predominantly driven by an increased salience of self- compared to externally determined action outcomes or whether differences in the perceived instrumental value of outcomes contribute to outcome monitoring in goal-directed tasks. To test this, we recorded electroencephalography while participants performed a reinforcement learning task involving free choices, action-relevant forced choices, and action-irrelevant forced choices. We observed larger midfrontal theta power and N100 amplitudes for feedback following free choices compared with action-relevant and action-irrelevant forced choices. In addition, a Reward Positivity was only present for free but not forced choice outcomes. Crucially, our results indicate that enhanced outcome processing is not driven by the relevance of outcomes for future actions but rather stems from the association of outcomes with recent self-determined choice. Our findings highlight the pivotal role of self-determination in tracking the consequences of our actions and contribute to an understanding of the cognitive processes underlying the choice-induced facilitation in outcome monitoring.

Different Faces of Medial Beta-Band Activity Reflect Distinct Visuomotor Feedback Signals.

Beta-band (13-35 Hz) modulations following reward, task outcome feedback, and error have been described in cognitive and/or motor adaptation tasks. Observations from different studies are, however, difficult to conciliate. Among the studies that used cognitive response selection tasks, several reported an increase in beta-band activity following reward, whereas others observed increased beta power after negative feedback. Moreover, in motor adaptation tasks, an attenuation of the postmovement beta rebound follows a movement execution error induced by visual or mechanical perturbations. Given that kinematic error typically leads to negative task-outcome feedback (e.g., target missed), one may wonder how contradictory modulations, beta power decrease with movement error versus beta power increase with negative feedback, may coexist. We designed a motor adaptation task in which female and male participants experience varied feedbacks-binary success/failure feedback, kinematic error, and sensory-prediction error-and demonstrate that beta-band modulations in opposite directions coexist at different spatial locations, time windows, and frequency ranges. First, high beta power in the medial frontal cortex showed opposite modulations well separated in time when compared in success and failure trials; that is, power was higher in success trials just after the binary success feedback, whereas it was lower in the postmovement period compared with failure trials. Second, although medial frontal high-beta activity was sensitive to task outcome, low-beta power in the medial parietal cortex was strongly attenuated following movement execution error but was not affected by either the outcome of the task or sensory-prediction error. These findings suggest that medial beta activity in different spatio-temporal-spectral configurations play a multifaceted role in encoding qualitatively distinct feedback signals.SIGNIFICANCE STATEMENT Beta-band activity reflects neural processes well beyond sensorimotor functions, including cognition and motivation. By disentangling alternative spatio-temporal-spectral patterns of possible beta-oscillatory activity, we reconcile a seemingly discrepant literature. First, high-beta power in the medial frontal cortex showed opposite modulations separated in time in success and failure trials; power was higher in success trials just after success feedback and lower in the postmovement period compared with failure trials. Second, although medial frontal high-beta activity was sensitive to task outcome, low-beta power in the medial parietal cortex was strongly attenuated following movement execution error but was not affected by the task outcome or the sensory-prediction error. We propose that medial beta activity reflects distinct feedback signals depending on its anatomic location, time window, and frequency range.

Dorsal posterior cingulate cortex responds to negative feedback information supporting learning and relearning of response policies.

Many challenges in life come without explicit instructions. Instead, humans need to test, select, and adapt their behavioral responses based on feedback from the environment. While reward-centric accounts of feedback processing primarily stress the reinforcing aspect of positive feedback, feedback's central function from an information-processing perspective is to offer an opportunity to correct errors, thus putting a greater emphasis on the informational content of negative feedback. Independent of its potential rewarding value, the informational value of performance feedback has recently been suggested to be neurophysiologically encoded in the dorsal portion of the posterior cingulate cortex (dPCC). To further test this association, we investigated multidimensional categorization and reversal learning by comparing negative and positive feedback in an event-related functional magnetic resonance imaging experiment. Negative feedback, compared with positive feedback, increased activation in the dPCC as well as in brain regions typically involved in error processing. Only in the dPCC, subarea d23, this effect was significantly enhanced in relearning, where negative feedback signaled the need to shift away from a previously established response policy. Together with previous findings, this result contributes to a more fine-grained functional parcellation of PCC subregions and supports the dPCC's involvement in the adaptation to behaviorally relevant information from the environment.

Directed information exchange between cortical layers in macaque V1 and V4 and its modulation by selective attention.

Achieving behavioral goals requires integration of sensory and cognitive information across cortical laminae and cortical regions. How this computation is performed remains unknown. Using local field potential recordings and spectrally resolved conditional Granger causality (cGC) analysis, we mapped visual information flow, and its attentional modulation, between cortical layers within and between macaque brain areas V1 and V4. Stimulus-induced interlaminar information flow within V1 dominated upwardly, channeling information toward supragranular corticocortical output layers. Within V4, information flow dominated from granular to supragranular layers, but interactions between supragranular and infragranular layers dominated downwardly. Low-frequency across-area communication was stronger from V4 to V1, with little layer specificity. Gamma-band communication was stronger in the feedforward V1-to-V4 direction. Attention to the receptive field of V1 decreased communication between all V1 layers, except for granular-to-supragranular layer interactions. Communication within V4, and from V1 to V4, increased with attention across all frequencies. While communication from V4 to V1 was stronger in lower-frequency bands (4 to 25 Hz), attention modulated cGCs from V4 to V1 across all investigated frequencies. Our data show that top-down cognitive processes result in reduced communication within cortical areas, increased feedforward communication across all frequency bands, and increased gamma-band feedback communication.

Getting off track: Cortical feedback processing network modulated by continuous error signal during target-feedback mismatch.

Performance monitoring and feedback processing - especially in the wake of erroneous outcomes - represent a crucial aspect of everyday life, allowing us to deal with imminent threats in the short term but also promoting necessary behavioral adjustments in the long term to avoid future conflicts. Over the last thirty years, research extensively analyzed the neural correlates of processing discrete error stimuli, unveiling the error-related negativity (ERN) and error positivity (Pe) as two main components of the cognitive response. However, the connection between the ERN/Pe and distinct stages of error processing, ranging from action monitoring to subsequent corrective behavior, remains ambiguous. Furthermore, mundane actions such as steering a vehicle already transgress the scope of discrete erroneous events and demand fine-tuned feedback control, and thus, the processing of continuous error signals - a topic scarcely researched at present. We analyzed two electroencephalography datasets to investigate the processing of continuous erroneous signals during a target tracking task, employing feedback in various levels and modalities. We observed significant differences between correct (slightly delayed) and erroneous feedback conditions in the larger one of the two datasets that we analyzed, both in sensor and source space. Furthermore, we found strong error-induced modulations that appeared consistent across datasets and error conditions, indicating a clear order of engagement of specific brain regions that correspond to individual components of error processing.

Infants' visual perception without feature-binding.

We reveal a unique visual perception before feature-integration of colour and motion in infants. Visual perception is established by the integration of multiple features, such as colour and motion direction. The mechanism of feature integration benefits from the ongoing interplay between feedforward and feedback loops, yet our comprehension of this causal connection remains incomplete. Researchers have explored the role of recurrent processing in feature integration by studying a visual illusion called 'misbinding', wherein visual characteristics are erroneously merged, resulting in a perception distinct from the originally presented stimuli. Anatomical investigations have revealed that the neural pathways responsible for recurrent connections are underdeveloped in early infants. Therefore, there is a possibility that younger infants could potentially perceive the physically presented visual information that adults miss due to misbinding. Here, we demonstrate that infants less than half a year old showed no misbinding; thus, they perceived the physically presented visual information, while infants more than half a year old perceived incorrectly integrated visual information, showing misbinding. Our findings indicate that recurrent processing barely functions in infants younger than six months of age and that visual information that should have been originally integrated is perceived as it is without being integrated.

Disentangling performance-monitoring signals encoded in feedback-related EEG dynamics.

The feedback-related negativity (FRN) is a well-established electrophysiological correlate of feedback-processing. However, there is still an ongoing debate whether the FRN is driven by negative or positive reward prediction errors (RPE), valence of feedback, or mere surprise. Our study disentangles independent contributions of valence, surprise, and RPE on the feedback-related neuronal signal including the FRN and P3 components using the statistical power of a sample of N = 992 healthy individuals. The participants performed a modified time-estimation task, while EEG from 64 scalp electrodes was recorded. Our results show that valence coding is present during the FRN with larger amplitudes for negative feedback. The FRN is further modulated by surprise in a valence-dependent way being more positive-going for surprising positive outcomes. The P3 was strongly driven by both global and local surprise, with larger amplitudes for unexpected feedback and local deviants. Behavioral adaptations after feedback and FRN just show small associations. Results support the theory of the FRN as a representation of a signed RPE. Additionally, our data indicates that surprising positive feedback enhances the EEG response in the time window of the P3. These results corroborate previous findings linking the P3 to the evaluation of PEs in decision making and learning tasks.

Modulating social feedback processing by deep TMS targeting the medial prefrontal cortex: Behavioral and electrophysiological manifestations.

Neuroimaging studies have suggested that the medial prefrontal cortex (mPFC) is a key brain region for social feedback processing, but previous findings are largely based on correlational approaches. In this study, we use the deep transcranial magnetic stimulation (dTMS) to manipulate mPFC activity, then investigate participants' behavioral performance and event-related potentials (ERPs) during the Social Judgment Paradigm. A between-subject design was applied, such that both the active dTMS group and the sham group consisted of 30 participants. We found that the sham group was more likely to predict that they would be socially accepted (rather than rejected) by peers, but the same was not true in the active group. Additionally, this study is the first one to observe ERP signal changes in response to dTMS manipulation. ERP results show that both the expectation stage and the experience stage of social feedback processing were modulated by dTMS: (1) at the expectation stage, the P1 component was smaller in the active group than the sham group, while the stimulus-preceding negativity showed a stronger differentiating effect between positive and negative prediction in the sham group than the active group; (2) at the experience stage, the sensitivity of the late positive potential to the valence and predictability of social feedback was stronger in the sham group than the active group. These results improve our understanding about the relationship between the mPFC and social feedback processing.

Non-stimulated regions in early visual cortex encode the contents of conscious visual perception.

Predictions shape our perception. The theory of predictive processing poses that our brains make sense of incoming sensory input by generating predictions, which are sent back from higher to lower levels of the processing hierarchy. These predictions are based on our internal model of the world and enable inferences about the hidden causes of the sensory input data. It has been proposed that conscious perception corresponds to the currently most probable internal model of the world. Accordingly, predictions influencing conscious perception should be fed back from higher to lower levels of the processing hierarchy. Here, we used functional magnetic resonance imaging and multivoxel pattern analysis to show that non-stimulated regions of early visual areas contain information about the conscious perception of an ambiguous visual stimulus. These results indicate that early sensory cortices in the human brain receive predictive feedback signals that reflect the current contents of conscious perception.

The impact of subclinical neck pain on goal-directed upper limb movement in the horizontal plane.

Subclinical neck pain (SCNP) refers to recurrent neck pain and/or stiffness for which individuals have not yet sought treatment. Prior studies have shown that individuals with SCNP have altered cerebellar processing that exhibits an altered body schema. The cerebellum also plays a vital role in upper limb reaching movements through refining internal models and integrating sensorimotor information. However, the impact of SCNP on these processes has yet to be examined in the context of a rapid goal-directed aiming response that relies on feedforward and feedback processes to guide the limb to the target. To address this, SCNP and control participants performed goal-directed upper limb movements with the dominant and non-dominant hands using light and heavy styli in the horizontal plane. The results show greater peak accelerations in SCNP participants using the heavy stylus. However, there were no other group differences seen, possibly due to the fact that reaching behavior predominantly relies on vision such that any proprioceptive deficits seen in those with SCNP can be compensated. This study illustrates the robust compensatory nature of the CNS when performing end-effector reaching tasks, suggesting studies altering visual feedback may be needed to see the full impact of SCNP on upper limb aiming.

The influence of internal models on feedback-related brain activity.

Decision making relies on the interplay between two distinct learning mechanisms, namely habitual model-free learning and goal-directed model-based learning. Recent literature suggests that this interplay is significantly shaped by the environmental structure as represented by an internal model. We employed a modified two-stage but one-decision Markov decision task to investigate how two internal models differing in the predictability of stage transitions influence the neural correlates of feedback processing. Our results demonstrate that fronto-central theta and the feedback-related negativity (FRN), two correlates of reward prediction errors in the medial frontal cortex, are independent of the internal representations of the environmental structure. In contrast, centro-parietal delta and the P3, two correlates possibly reflecting feedback evaluation in working memory, were highly susceptible to the underlying internal model. Model-based analyses of single-trial activity showed a comparable pattern, indicating that while the computation of unsigned reward prediction errors is represented by theta and the FRN irrespective of the internal models, the P3 adapts to the internal representation of an environment. Our findings further substantiate the assumption that the feedback-locked components under investigation reflect distinct mechanisms of feedback processing and that different internal models selectively influence these mechanisms.

Correlations Between Primary Motor Cortex Activity with Recent Past and Future Limb Motion During Unperturbed Reaching.

Many studies highlight that human movements are highly successful yet display a surprising amount of variability from trial to trial. There is a consistent pattern of variability throughout movement: initial motor errors are corrected by the end of movement, suggesting the presence of a powerful online control process. Here, we analyze the trial-by-trial variability of goal-directed reaching in nonhuman primates (five male Rhesus monkeys) and demonstrate that they display a similar pattern of variability during reaching, including a strong negative correlation between initial and late hand motion. We then demonstrate that trial-to-trial neural variability of primary motor cortex (M1) is positively correlated with variability of future hand motion (τ = ∼160 ms) during reaching. Furthermore, the variability of M1 activity is also correlated with variability of past hand motion (τ = ∼90 ms), but in the opposite polarity (i.e., negative correlation). Partial correlation analysis demonstrated that M1 activity independently reflects the variability of both past and future hand motions. These findings provide support for the hypothesis that M1 activity is involved in online feedback control of motor actions.SIGNIFICANCE STATEMENT Previous studies highlight that primary motor cortex (M1) rapidly responds to either visual or mechanical disturbances, suggesting its involvement in online feedback control. However, these studies required external disturbances to the motor system and it is not clear whether a similar feedback process addresses internal noise/errors generated by the motor system itself. Here, we introduce a novel analysis that evaluates how variations in the activity of M1 neurons covary with variations in hand motion on a trial-to-trial basis. The analyses demonstrate that M1 activity is correlated with hand motion in both the near future and the recent past, but with opposite polarity. These results suggest that M1 is involved in online feedback motor control to address errors/noise within the motor system.

Benchmarking laminar fMRI: Neuronal spiking and synaptic activity during top-down and bottom-up processing in the different layers of cortex.

High resolution laminar fMRI is beginning to probe responses in the different layers of cortex. What can we expect this exciting new technique to discover about cortical processing and how can we verify that it is producing an accurate picture of the underlying laminar differences in neural processing? This review will address our knowledge of laminar cortical circuitry gained from electrophysiological studies in macaque monkeys with a focus on the primary visual cortex, as this area has been most often targeted in both laminar electrophysiological and fMRI studies. We will review how recent studies are attempting to verify the accuracy of laminar fMRI by recreating the known laminar profiles of various neural tuning properties. Furthermore, we will examine how feedforward and feedback-related neural processes engage different cortical layers, producing canonical patterns of spiking and synaptic activity as estimated by the analysis of current-source density. These results provide a benchmark for recent studies aiming to examine the profiles of bottom-up and top-down processes with laminar fMRI. Finally, we will highlight particularly useful paradigms and approaches which may help us to understand processing in the different layers of the human cerebral cortex.

Altered Oscillatory Responses to Feedback in Borderline Personality Disorder are Linked to Symptom Severity.

Several studies using electroencephalography (EEG) demonstrate that the processing of feedback in patients suffering from borderline personality disorder (BPD) is altered in comparison to healthy controls. Differences occur in the theta (ca. 5 Hz) and high-beta frequency-ranges (ca. 20 Hz) of oscillations in response to negative and positive feedback, respectively. However, alpha (ca. 10 Hz) and low-beta (ca. 15 Hz) oscillations have also been shown to be involved in feedback processing. We hypothesized that additional alterations might occur in these frequency ranges in BPD. Eighteen patients with BPD and twenty-two healthy controls performed a gambling task while 64-channel-EEG was recorded. Induced oscillatory responses to positive (i.e. gain) and negative (i.e. loss) feedback in the alpha and low-beta frequency range were investigated. No significant differences were found in the alpha frequency range. Regarding the low-beta frequency range a significant Group (i.e. BPD vs. healthy controls) × Valence (i.e. gain vs. loss) interaction in the time frame between 600 and 700 milliseconds after feedback was found. This effect showed a significant correlation with symptom severity (assessed with the BSL-23). The results indicate that feedback processing in BPD could be more heavily altered than previously expected, with more severe symptomatology being linked to stronger alterations in oscillatory responses to feedback in the low-beta range.

Frontal cortex electrophysiology in reward- and punishment-related feedback processing during advice-guided decision making: An interleaved EEG-DC stimulation study.

During decision making, individuals are prone to rely on external cues such as expert advice when the outcome is not known. However, the electrophysiological correlates associated with outcome uncertainty and the use of expert advice are not completely understood. The feedback-related negativity (FRN), P3a, and P3b are event-related brain potentials (ERPs) linked to dissociable stages of feedback and attentional processing during decision making. Even though these ERPs are influenced by both reward- and punishment-related feedback, it remains unclear how extrinsic information during uncertainty modulates these brain potentials. In this study, the effects of advice cues on decision making were investigated in two separate experiments. In the first experiment, electroencephalography (EEG) was recorded in healthy volunteers during a decision-making task in which the participants received reward or punishment feedback preceded by novice, amateur, or expert advice. The results showed that the P3a component was significantly influenced by the subjective predictive value of an advice cue, whereas the FRN and P3b were unaffected by the advice cues. In the second, sham-controlled experiment, cathodal transcranial direct current stimulation (ctDCS) was administered in conjunction with EEG in order to explore the direct contributions of the frontal cortex to these brain potentials. Results showed no significant change in either advice-following behavior or decision times. However, ctDCS did decrease FRN amplitudes as compared to sham, with no effect on the P3a or P3b. Together, these findings suggest that advice information may act primarily on attention allocation during feedback processing, whereas the electrophysiological correlates of the detection and updating of internal prediction models are not affected.

The role of the cerebellum for feedback processing and behavioral switching in a reversal-learning task.

Previous studies have reported cerebellar activations during error and reward processing. The present study investigated if the cerebellum differentially processes feedback depending on changes in response strategy during reversal learning, as is conceivable given its internal models for movement and thought. Negative relative to positive feedback in an fMRI-based reversal learning task was hypothesized to be associated with increased cerebellar activations. Moreover, increased activations were expected for negative feedback followed by a change in response strategy compared to negative feedback not followed by such a change, and for first positive feedback after compared to final negative feedback before a change, due to updating of internal models. As predicted, activation in lobules VI and VIIa/Crus I was increased for negative relative to positive feedback, and for final negative feedback before a change in response strategy relative to negative feedback not associated with a change. Moreover, activation was increased for first positive feedback after relative to final negative feedback before a change. These findings are consistent with updating of cerebellar internal models to accommodate new behavioral strategies. Recruitment of posterior regions in reversal learning is in line with the cerebellar functional topography, with posterior regions involved in complex motor and cognitive functions.

Look who's judging-Feedback source modulates brain activation to performance feedback in social anxiety.

It is as yet unknown if behavioral and neural correlates of performance monitoring in socially anxious individuals are affected by whether feedback is provided by a person or a computer. This fMRI study investigated modulation of feedback processing by feedback source (person vs. computer) in participants with high (HSA) (N=16) and low social anxiety (LSA) (N=16). Subjects performed a choice task in which they were informed that they would receive positive or negative feedback from a person or the computer. Subjective ratings indicated increased arousal and anxiety in HSA versus LSA, most pronounced for social and negative feedback. FMRI analyses yielded hyperactivation in ventral medial prefrontal cortex (vmPFC)/anterior cingulate cortex (ACC) and insula for social relative to computer feedback, and in mPFC/ventral ACC for positive relative to negative feedback in HSA as compared to LSA. These activation patterns are consistent with increased interoception and self-referential processing in social anxiety, especially during processing of positive feedback. Increased ACC activation in HSA to positive feedback may link to unexpectedness of (social) praise as posited in social anxiety disorder (SAD) psychopathology. Activation in rostral ACC showed a reversed pattern, with decreased activation to positive feedback in HSA, possibly indicating altered action values depending on feedback source and valence. The present findings corroborate a crucial role of mPFC for performance monitoring in social anxiety.

Processing of Positive and Negative Feedback in Patients with Cerebellar Lesions.

It is well accepted that the cerebellum plays a crucial role in the prediction of the sensory consequences of movements. Recent findings of altered error processing in patients with selective cerebellar lesions led to the hypothesis that feedback processing and feedback-based learning might be affected by cerebellar damage as well. Thus, the present study investigated learning from and processing of positive and negative feedback in 12 patients with selective cerebellar lesions and healthy control subjects. Participants performed a monetary feedback learning task. The processing of positive and negative feedback was assessed by means of event-related potentials (ERPs) during the learning task and during a separate task in which the frequencies of positive and negative feedback were balanced. Patients did not show a general learning deficit compared to controls. Relative to the control group, however, patients with cerebellar lesions showed significantly higher ERP difference wave amplitudes (rewards-losses) in a time window between 250 and 450 ms after feedback presentation, possibly indicating impaired outcome prediction. The analysis of the original waveforms suggested that patients and controls primarily differed in their pattern of feedback-related negativity and P300 amplitudes. Our results add to recent findings on altered performance monitoring associated with cerebellar damage and demonstrate, for the first time, alterations of feedback processing in patients with cerebellar damage. Unaffected learning performance appears to suggest that chronic cerebellar lesions can be compensated in behaviour.

Effects of invalid feedback on learning and feedback-related brain activity in decision-making.

For adaptive decision-making it is important to utilize only relevant, valid and to ignore irrelevant feedback. The present study investigated how feedback processing in decision-making is impaired when relevant feedback is combined with irrelevant and potentially invalid feedback. We analyzed two electrophysiological markers of feedback processing, the feedback-related negativity (FRN) and the P300, in a simple decision-making task, in which participants processed feedback stimuli consisting of relevant and irrelevant feedback provided by the color and meaning of a Stroop stimulus. We found that invalid, irrelevant feedback not only impaired learning, it also altered the amplitude of the P300 to relevant feedback, suggesting an interfering effect of irrelevant feedback on the processing of relevant feedback. In contrast, no such effect on the FRN was obtained. These results indicate that detrimental effects of invalid, irrelevant feedback result from failures of controlled feedback processing.

Detecting concealed information using feedback related event-related brain potentials.

Employing an event-related potential (ERP)-based concealed information test (CIT), the present study investigated (1) the neurocognitive processes when people received feedbacks regarding their deceptive/truthful responses and (2) whether such feedback-related ERP activities can be used to detect concealed information above and beyond the recognition-related P300. During the CIT, participants were presented with rare, meaningful probes (their own names) embedded within a series of frequent yet meaningless irrelevants (others' names). Participants were instructed to deny their recognition of the probes. Critically, following participants' responses, they were provided with feedbacks regarding whether they succeeded or failed in the CIT. Replicating previous ERP-based CITs, we found a larger P300 elicited by probe compared to irrelevant. Regarding feedback-related ERPs, a temporospatial Principle Component Analyses found two ERP components that were not only sensitive to feedback manipulations but also can discriminate probe from irrelevant: an earlier, central-distributed positivity that was elicited by "success" feedbacks peaked around 219ms; and a later, right central-distributed positivity that was also elicited by "success" feedbacks, peaked around 400ms. Importantly, the feedback ERPs were not correlated with P300 that was elicited by probe/irrelevant, suggesting that these two ERPs reflect independent processes underlying memory concealment. These findings illustrate the feasibility and promise of using feedback-related ERPs to detect concealed memory and thus deception.