Pain by mistake:investigating a link between error-related negativity and pain avoidance behavior

ABSTRACT: Pain can be considered as a signal of "bodily error": Errors put organisms at danger and activate behavioral defensive systems. If the error is of physical nature, pain is the warning signal that motivates protective action such as avoidance behavior to safeguard our body's integrity. Interestingly, an important component of neural error processing, the error-related negativity (ERN), has been found to be related to avoidance in anxiety disorders. The present study is the first to extend these findings to pain and investigate the relationship between ERN and pain-related avoidance behavior. It was hypothesized that individuals with larger ERN amplitudes would show more pain-related avoidance behavior and would be more persistent in their avoidance despite changes in the environment. Fifty-three healthy individuals performed the Eriksen Flanker task during which their brain activity upon correct and erroneous motor responses was recorded by means of high-density electroencephalography. Avoidance behavior was assessed with an arm-reaching task using the HapticMaster robot arm. Results showed that, in contrast to our hypothesis, avoidance was not related to ERN amplitudes. Surprisingly, persons with elevated ERN amplitudes showed low levels of avoidance specifically during early acquisition trials. In contrast to earlier findings in anxiety disorders, individuals with elevated ERN amplitudes did not engage in more pain-related avoidance behavior. In fact, the opposite pattern was found at the start of acquisition: individuals with higher compared to lower ERN amplitudes were slower in learning to avoid pain. Replications and future studies on the relationship between ERN and avoidance behavior are needed

The Impact of Unpredictability on Dyspnea Perception, Anxiety and Interoceptive Error Processing

Dyspnea is a prevalent interoceptive sensation and the aversive cardinal symptom in many cardiorespiratory diseases as well as in mental disorders. Especially the unpredictability of the occurrence of dyspnea episodes has been suggested to be highly anxiety provoking for affected patients. Moreover, previous studies demonstrated that unpredictable exteroceptive stimuli increased self-reports and electrophysiological responses of anxiety such as the startle probe N100 as well as amplified the processing of errors as reflected by greater error-related negativity (ERN). However, studies directly examining the role of unpredictability on dyspnea perception, anxiety, and error processing are widely absent. Using high-density electroencephalography, the present study investigated whether unpredictable compared to predictable dyspnea would increase the perception of dyspnea, anxiety and interoceptive error processing. Thirty-two healthy participants performed a respiratory forced choice reaction time task to elicit an interoceptive ERN during two conditions: an unpredictable and a predictable resistive load-induced dyspnea condition. Predictability was manipulated by pairing (predictable condition) or not pairing (unpredictable condition) dyspnea with a startle tone probe. Self-reports of dyspnea and affective state as well as the startle probe N100 and interoceptive ERN were measured. The results demonstrated greater dyspnea unpleasantness in the unpredictable compared to the predictable condition. Post hoc analyses revealed that this was paralleled by greater anxiety, and greater amplitudes for the startle probe N100 and the interoceptive ERN during the unpredictable relative to the predictable condition, but only when the unpredictable condition was experienced in the first experimental block. Furthermore, higher trait-like anxiety sensitivity was associated with higher ratings for dyspnea unpleasantness and experimental state anxiety ratings. The present findings suggest that unpredictability increases the perception of dyspnea unpleasantness. This effect seems related to increased state and trait anxiety and interoceptive error processing, especially when upcoming dyspnea is particularly unpredictable, such as in early experimental phases. Future studies are required to further substantiate these findings in patients suffering from dyspnea

Aversiveness of errors in performance monitoring and error related negativity in obsessive compulsive symptomatology

The error-related negativity is one of the most examined event-related potentials in the study of cognitive control, yet its functional significance has not been fully determined. The present dissertation had the objective to investigate the relationship between error processing and affective states manipulations in non-clinical samples and in OC symptomatology. Two studies constitute this dissertation. In study 1, we conducted a systematic review of studies investigating affective state manipulations, aversiveness of errors and the ERN. This review showed considerable evidence for ERN sensitivity to affect states experimental manipulations. In study 2, we aimed to explore the incidence of the error-related potentials at a gambling-type task (HiLo game) in a sample composed of people with high OCD symptomatology. Although the ERPs of interest were not elicited, we showed that the HiLo game is a promising paradigm to investigate the ERN in upcoming studies. In the general discussion, the results from the two studies are discussed in relation to the literature on error monitoring and affective conceptualizations

Symptoms of depersonalisation/derealisation disorder as measured by brain electrical activity: A systematic review

Depersonalisation/derealisation disorder (DPD) refers to frequent and persistent detachment from bodily self and disengagement from the outside world. As a dissociative disorder, DPD affects 1–2 % of the population, but takes 7–12 years on average to be accurately diagnosed. In this systematic review, we comprehensively describe research targeting the neural correlates of core DPD symptoms, covering publications between 1992 and 2020 that have used electrophysiological techniques. The aim was to investigate the diagnostic potential of these relatively inexpensive and convenient neuroimaging tools. We review the EEG power spectrum, components of the event-related potential (ERP), as well as vestibular and heartbeat evoked potentials as likely electrophysiological biomarkers to study DPD symptoms. We argue that acute anxiety- or trauma-related impairments in the integration of interoceptive and exteroceptive signals play a key role in the formation of DPD symptoms, and that future research needs analysis methods that can take this integration into account. We suggest tools for prospective studies of electrophysiological DPD biomarkers, which are urgently needed to fully develop their diagnostic potential

Electrocortical underpinnings of error monitoring in health and pathology

It becomes clear from the literature described above (Chapter 1), that the error monitoring mechanisms play a fundamental role in signalling the need for cognitive control. Many studies already provided a consistent evidence on the existence of peculiar ways in which the brain signals this need through electrophysiological changes. However, the following set of empirical studies aims to gain further insight into these complex processes by measuring brain activity changes in situations that alter the way one experience errors. The second Chapter (Chapter 2) consists of a brief commentary that was made in response to an article on the brain activity to action errors. In this commentary we propose new possibilities to explore our topic of interest, by taking advantage of EEG and modern virtual reality facilities. The thesis includes three EEG-VR studies: one on the error-mechanism in healthy participants (Chapter 3) and two studies on error monitoring system in pathological populations (Chapter 4, 5), as main parts of the core of the thesis. As a collateral project, in the Appendix, there is an EEG study on action observation in elite players (Chapter 7). In the first study (Chapter 3), we investigated a very simple but fundamental question. As we saw in the introduction, error-related signatures are evoked when an error occurs. But it is not clear how much of this is due to the occurrence of a violation of the intended goal or simply to the observation of a rare – thus less predictable – event. To this aim, we used a paradigm developed in the former years in our laboratory (Pavone et al., 2016; Spinelli et al., 2017), characterized by a setup in immersive Virtual Reality (VR) and simultaneous EEG recording. Building on the previous findings, we designed an EEG-VR study in which we manipulated the probability of observing errors in actions. In another study (Chapter 4) we investigated how erroneous actions are experienced by people with brain damage and diagnosis of Apraxia. Apraxic patients are people with hemispheric lesions and defective awareness on a variety of aspects that cover perceptuo-motor, cognitive or emotional domains. This study was developed after the results obtained by Canzano and colleagues (2014) in a behavioral study in which apraxic patients were asked to imitate the actions executed by the experimenter and judge their correctness; results revealed that bucco-facial apraxic patients manifest a specific deficit in detecting their own gestural errors when they are explicitly asked to judge them. With the present study we wanted to investigate apraxic brain’ response to action errors, while they embody an avatar in first person perspective (EEG-VR setup). The third study (Chapter 5) investigates the integrity of the error-monitoring system in Parkinson’s Disease and the impact of the dopaminergic treatment in the brain response to errors. To this aim we used the proposed VR action-observation paradigm, in which Parkinson patients observed successful and unsuccessful reach-to-grasp actions in first person perspective while EEG activity was recorded; the same patients were tested while being under dopaminergic treatment and during a dopaminergic withdrawal state. In another chapter we provide a critical overview of the findings of this work (General Discussion, Chapter 6). In the last chapter, the Appendix (Chapter 7), there is a collateral project of another research line of the Laboratory, in which I have being involved. In this study we are investigating the cortical underpinning of elite players during observation of goal-directed actions, in their domain of expertise. We recorded the EEG activity of elite wheelchair basketball players while observing free-throws performed by paraplegic athletes. We expected their brain correlates to be different from novice players and to be able to easily discriminate whether a basketball shot would be successful or unsuccessful (project still ongoing)

Performance monitoring during action observation and auditory lexical decisions

How does the brain monitor performances? Does expertise modulate this process? How does an observer’s error related activity differ from a performers own error related activity? How does ambiguity change the markers of error monitoring? In this thesis, I present two EEG studies and a commentary that sought to answer these questions. Both empirical studies concern performance monitoring in two different contexts and from two different personal perspectives, i.e. investigating the effects of expertise on electroencephalographic (EEG) neuromarkers of performance monitoring and in terms of monitoring own and others’ errors during actions and language processing. My first study focused on characterizing the electrophysiological responses in experts and control individuals while they are observing domain-specific actions in wheelchair basketball with correct and wrong outcomes (Chapter II). The aim of the commentary in the following chapter was to highlight the role of Virtual Reality approaches to error prediction during one’s own actions (Chapter III). The fourth chapter hypothesised that the error monitoring markers are present during both one’s own performance errors in a lexical decision task, and the observation of others’ performance errors (Chapter IV), however, the results suggested a further modulation of uncertainty created by our task design. The final chapter presents a general discussion that provides an overview of the results of my PhD work (Chapter V). The present chapter consists of a literature review in the leading frameworks of performance monitoring, action observation, visuo-motor expertise and language processing

The error-related negativity for error processing in interoception

The error-related negativity (ERN) is an event-related potential in the electroencephalogram (EEG) observed within the first 100 ms after commission of an error. Increased ERN amplitudes have been observed in several psychological disorders characterized by high negative affect. While the ERN has extensively been studied in tasks using exteroceptive stimuli, its relation to interoceptive stimuli is unknown. Since errors related to interoception might be particularly relevant for survival and negative affect, this study aimed to explore the ERN for errors related to interoceptive, respiratory sensations (intERN). Moreover, we compared the intERN with a commonly observed ERN related to exteroceptive, visual stimuli (extERN) and examined their associations with interoception-related negative affect. We studied the ERN using a respiratory occlusion task (intERN) and a visual flanker task (extERN) in 40 healthy volunteers during continuous 129 channel EEG recordings. In the occlusion task, participants received inspiratory occlusions of two different durations and indicated whether each occlusion was short or long. In the Flanker task, participants indicated the direction of arrowheads. Interoception-related negative affect was assessed with the Anxiety Sensitivity Index. Comparable with the extERN, the intERN was observed at fronto-central scalp positions after error commission in the occlusion task, but it peaked significantly earlier than the extERN. Mean amplitudes of the intERN and extERN showed no significant difference and were not correlated. Moreover, higher levels of anxiety sensitivity were correlated with significantly greater amplitudes of the intERN, but with lower amplitudes of the extERN. The present results firstly demonstrate an error-related negativity EEG-potential that is related to interoceptive sensations (intERN). This intERN is not associated with a commonly observed ERN elicited by exteroceptive stimuli and is distinctly linked to higher levels of interoceptionrelated negative affect. The intERN might be a promising neural marker for future studies on interoception, negative affect and error processing.status: publishe