Olave E. Krigolson

The feedback correct-related positivity: Sensitivity of the event-related brain potential to unexpected positive feedback

The N200 and the feedback error-related negativity (fERN) are two components of the event-related brain potential (ERP) that share similar scalp distributions, time courses, morphologies, and functional dependencies, which raises the question as to whether they are actually the same phenomenon. To investigate this issue, we recorded the ERP from participants engaged in two tasks that independently elicited the N200 and fERN. Our results indicate that they are, in fact, the same ERP component and further suggest that positive feedback elicits a positive-going deflection in the time range of the fERN. Taken together, these results indicate that negative feedback elicits a common N200 and that modulation of fERN amplitude results from the superposition on correct trials of a positive-going deflection that we term the feedback correct-related positivity.

When is an error not a prediction error? An electrophysiological investigation

A recent theory holds that the anterior cingulate cortex (ACC) uses reinforcement learning signals conveyed by the midbrain dopamine system to facilitate flexible action selection. According to this position, the impact of reward prediction error signals on ACC modulates the amplitude of a component of the event-related brain potential called the error-related negativity (ERN). The theory predicts that ERN amplitude is monotonically related to the expectedness of the event: It is larger for unexpected outcomes than for expected outcomes. However, a recent failure to confirm this prediction has called the theory into question. In the present article, we investigated this discrepancy in three trial-and-error learning experiments. All three experiments provided support for the theory, but the effect sizes were largest when an optimal response strategy could actually be learned. This observation suggests that ACC utilizes dopamine reward prediction error signals for adaptive decision making when the optimal behavior is, in fact, learnable.

Reward positivity elicited by predictive cues.

A recent theory holds that a component of the human event-related brain potential called the reward positivity reflects a reward prediction error signal. We investigated this idea in gambling-like task in which, on each trial, a visual stimulus predicted a subsequent rewarding or nonrewarding outcome with 80% probability. Consistent with earlier results, we found that the reward positivity was larger to unexpected than to expected outcomes. In addition, we found that the predictive cues also elicited a reward positivity, as proposed by the theory. These results indicate that the reward positivity reflects the initial assessment of whether a trial will end in success or failure and the reappraisal of that information once the outcome actually occurs.

Learning to become an expert: Reinforcement learning and the acquisition of perceptual expertise

To elucidate the neural mechanisms underlying the development of perceptual expertise, we recorded ERPs while participants performed a categorization task. We found that as participants learned to discriminate computer generated “blob” stimuli, feedback modulated the amplitude of the error-related negativity (ERN)—an ERP component thought to reflect error evaluation within medial–frontal cortex. As participants improved at the categorization task, we also observed an increase in amplitude of an ERP component associated with object recognition (the N250). The increase in N250 amplitude preceded an increase in amplitude of an ERN component associated with internal error evaluation (the response ERN). Importantly, these electroencephalographic changes were not observed for participants who failed to improve on the categorization task. Our results suggest that the acquisition of perceptual expertise relies on interactions between the posterior perceptual system and the reinforcement learning system involving medial–frontal cortex.

Choosing MUSE: Validation of a Low-Cost, Portable EEG System for ERP Research

In recent years there has been an increase in the number of portable low-cost electroencephalographic (EEG) systems available to researchers. However, to date the validation of the use of low-cost EEG systems has focused on continuous recording of EEG data and/or the replication of large system EEG setups reliant on event-markers to afford examination of event-related brain potentials (ERP). Here, we demonstrate that it is possible to conduct ERP research without being reliant on event markers using a portable MUSE EEG system and a single computer. Specifically, we report the results of two experiments using data collected with the MUSE EEG system—one using the well-known visual oddball paradigm and the other using a standard reward-learning task. Our results demonstrate that we could observe and quantify the N200 and P300 ERP components in the visual oddball task and the reward positivity (the mirror opposite component to the feedback-related negativity) in the reward-learning task. Specifically, single sample t-tests of component existence (all ps < 0.05), computation of Bayesian credible intervals, and 95% confidence intervals all statistically verified the existence of the N200, P300, and reward positivity in all analyses. We provide with this research paper an open source website with all the instructions, methods, and software to replicate our findings and to provide researchers with an easy way to use the MUSE EEG system for ERP research. Importantly, our work highlights that with a single computer and a portable EEG system such as the MUSE one can conduct ERP research with ease thus greatly extending the possible use of the ERP methodology to a variety of novel contexts.

The unidirectional prosaccade switch-cost: Electroencephalographic evidence of task-set inertia in oculomotor control

The execution of an antisaccade selectively increases the reaction time (RT) of a subsequent prosaccade (the unidirectional prosaccade switch-cost). To explain this finding, the task-set inertia hypothesis asserts that an antisaccade requires a cognitively mediated non-standard task-set that persists inertially and delays the planning of a subsequent prosaccade. The present study sought to directly test the theoretical tenets of the task-set inertia hypothesis by examining the concurrent behavioural and the event-related brain potential (ERP) data associated with the unidirectional prosaccade switch-cost. Participants pseudo-randomly alternated between pro- and antisaccades while electroencephalography (EEG) data were recorded. As expected, the completion of an antisaccade selectively increased the RT of a subsequent prosaccade, whereas the converse switch did not influence RTs. Thus, the behavioural results demonstrated the unidirectional prosaccade switch-cost. In terms of the ERP findings, we observed a reliable change in the amplitude of the P3 - time-locked to task-instructions - when trials were switched from a prosaccade to an antisaccade; however, no reliable change was observed when switching from an antisaccade to a prosaccade. This is a salient finding because extensive work has shown that the P3 provides a neural index of the task-set required to execute a to-be-completed response. As such, results showing that prosaccades completed after antisaccades exhibited increased RTs in combination with a P3 amplitude comparable to antisaccades provides convergent evidence that the unidirectional prosaccade switch-cost is attributed to the persistent activation of a non-standard antisaccade task-set.

Using brain potentials to understand prism adaptation: the error-related negativity and the P300

Prism adaptation (PA) is both a perceptual-motor learning task as well as a promising rehabilitation tool for visuo-spatial neglect (VSN)—a spatial attention disorder often experienced after stroke resulting in slowed and/or inaccurate motor responses to contralesional targets. During PA, individuals are exposed to prism-induced shifts of the visual-field while performing a visuo-guided reaching task. After adaptation, with goggles removed, visuomotor responding is shifted to the opposite direction of that initially induced by the prisms. This visuomotor aftereffect has been used to study visuomotor learning and adaptation and has been applied clinically to reduce VSN severity by improving motor responding to stimuli in contralesional (usually left-sided) space. In order to optimize PAs use for VSN patients, it is important to elucidate the neural and cognitive processes that alter visuomotor function during PA. In the present study, healthy young adults underwent PA while event-related potentials (ERPs) were recorded at the termination of each reach (screen-touch), then binned according to accuracy (hit vs. miss) and phase of exposure block (early, middle, late). Results show that two ERP components were evoked by screen-touch: an error-related negativity (ERN), and a P300. The ERN was consistently evoked on miss trials during adaptation, while the P300 amplitude was largest during the early phase of adaptation for both hit and miss trials. This study provides evidence of two neural signals sensitive to visual feedback during PA that may sub-serve changes in visuomotor responding. Prior ERP research suggests that the ERN reflects an error processing system in medial-frontal cortex, while the P300 is suggested to reflect a system for context updating and learning. Future research is needed to elucidate the role of these ERP components in improving visuomotor responses among individuals with VSN.

The role of visual processing in motor learning and control: Insights from electroencephalography

Traditionally our understanding of goal-directed action been derived from either behavioral findings or neuroanatomically derived imaging (i.e., fMRI). While both of these approaches have proven valuable, they lack the ability to determine a direct locus of function while concurrently having the necessary temporal precision needed to understand millisecond scale neural interactions respectively. In this review we summarize some seminal behavioral findings across three broad areas (target perturbation, feed-forward control, and feedback processing) and for each discuss the application of electroencephalography (EEG) to the understanding of the temporal nature of visual cue utilization during movement planning, control, and learning using four existing scalp potentials. Specifically, we examine the appropriateness of using the N100 potential as an indicator of corrective behaviors in response to target perturbation, the N200 as an index of movement planning, the P300 potential as a metric of feed-forward processes, and the feedback-related negativity as an index of motor learning. Although these existing components have potential for insight into cognitive contributions and the timing of the neural processes that contribute to motor control further research is needed to expand the control-related potentials and to develop methods to permit their accurate characterization across a wide range of behavioral tasks.

Event-related brain potentials during the visuomotor mental rotation task: The contingent negative variation scales to angle of rotation.

Perceptual judgments about the angular disparity of a character from its standard upright (i.e., mental rotation task) result in a concurrent increase in reaction time (RT) and modulation of the amplitude of the P300 event-related brain potential (ERP). It has therefore been proposed that the P300 represents the neural processes associated with a visual rotation. In turn, the visuomotor mental rotation (VMR) task requires reaching to a location that deviates from a target by a predetermined angle. Although the VMR task exhibits a linear increase in RT with increasing oblique angles of rotation, work has not examined whether the task is supported via a visual rotation analogous to its mental rotation task counterpart. This represents a notable issue because seminal work involving non-human primates has ascribed VMR performance to the motor-related rotation of directionally tuned neurons in the primary motor cortex. Here we examined the concurrent behavioral and ERP characteristics of a standard reaching task and VMR tasks of 35°, 70°, and 105° of rotation. Results showed that the P300 amplitude was larger for the standard compared to each VMR task--an effect independent of the angle of rotation. In turn, the amplitude of the contingent negative variation (CNV)--an ERP related to cognitive and visuomotor integration for movement preparation--was systematically modulated with angle of rotation. Thus, we propose that the CNV represents an ERP correlate related to the cognitive and/or visuomotor transformation demands of increasing the angular separation between a stimulus and a movement goal.

Event-related brain potentials and the study of reward processing: Methodological considerations

There is growing interest in using electroencephalography and specifically the event-related brain potential (ERP) methodology to study human reward processing. Since the discovery of the feedback related negativity (Miltner et al., 1997) and the development of theories associating the feedback related negativity and more recently the reward positivity with reinforcement learning, midbrain dopamine function, and the anterior cingulate cortex (i.e., Holroyd and Coles, 2002) researchers have used the ERP methodology to probe the neural basis of reward learning in humans. However, examination of the feedback related negativity and the reward positivity cannot be done without an understanding of some key methodological issues that must be taken into account when using ERPs and examining these ERP components. For example, even the component name - the feedback related negativity - is a source of debate within the research community as some now strongly feel that the component should be named the reward positivity (Proudfit, 2015). Here, ten key methodological issues are discussed - confusion in component naming, the reward positivity, component identification, peak quantification and the use of difference waveforms, frequency (the N200) and component contamination (the P300), the impact of feedback timing, action, and task learnability, and how learning results in changes in the amplitude of the feedback-related negativity/reward positivity. The hope here is to not provide a definitive approach for examining the feedback related negativity/reward positivity, but instead to outline the key issues that must be taken into account when examining this component to assist researchers in their study of human reward processing with the ERP methodology.