Greater neural responses to trajectory errors are associated with superior force field adaptation in older adults

Although age-related declines in cognitive, sensory and motor capacities are well documented, current evidence is mixed as to whether or not aging impairs sensorimotor adaptation to a novel dynamic environment. More importantly, the extent to which any deficits in sensorimotor adaptation are due to general impairments in neural plasticity, or impairments in the specific processes that drive adaptation is unclear. Here we investigated whether there are age-related differences in electrophysiological responses to reaching endpoint and trajectory errors caused by a novel force field, and whether markers of error processing relate to the ability of older adults to adapt their movements. Older and young adults (N = 24/group, both sexes) performed 600 reaches to visual targets, and received audio-visual feedback about task success or failure after each trial. A velocity-dependent curl field pushed the hand to one side during each reach. We extracted ERPs time-locked to movement onset [kinematic error-related negativity (kERN)], and the presentation of success/failure feedback [feedback error-related negativity (fERN)]. At a group level, older adults did not differ from young adults in the rate or extent of sensorimotor adaptation, but EEG responses to both trajectory errors and task errors were reduced in the older group. Most interestingly, the amplitude of the kERN correlated with the rate and extent of sensorimotor adaptation in older adults. Thus, older adults with an impaired capacity for encoding kinematic trajectory errors also have compromised abilities to adapt their movements in a novel dynamic environment

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

Bridging event-related potentials with behavioral studies in motor learning

Behavioral approaches and electrophysiology in understanding human sensorimotor systems have both yielded substantial advancements in past decades. In fact, behavioral neuroscientists have found that motor learning involves the two distinct processes of the implicit and the explicit. Separately, they have also distinguished two kinds of errors that drive motor learning: sensory prediction error and task error. Scientists in electrophysiology, in addition, have discovered two motor-related, event-related potentials (ERPs): error-related negativity (ERN), and feedback-related negativity (FRN). However, there has been a lack of interchange between the two lines of research. This article, therefore, will survey through the literature in both directions, attempting to establish a bridge between these two fruitful lines of research

Predictive monitoring of actions, EEG recordings in virtual reality

Error-related negativity (ERN) is a signal that is associated with error detection. Joch and colleagues (Joch M, Hegele M, Maurer H, Müller H, Maurer LK. J Neurophysiol 118: 486–495, 2017) successfully separated the ERN as a response to online prediction error from feedback updates. We discuss the role of ERN in action and suggest insights from virtual reality techniques; we consider the potential benefit of self-evaluation in determining the mechanisms of ERN amplitude; finally, we review the oscillatory activity that has been claimed to accompany ER

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)

Beyond passive observation: feedback anticipation and observation activate the mirror system in virtual finger movement control via P300-BCI

Action observation (AO) is widely used as a post-stroke therapy to activate sensorimotor circuits through the mirror neuron system. However, passive observation is often considered to be less effective and less interactive than goal-directed movement observation, leading to the suggestion that observation of goal-directed actions may have stronger therapeutic potential, as goal-directed AO has been shown to activate mechanisms for monitoring action errors. Some studies have also suggested the use of AO as a form of Brain–computer interface (BCI) feedback. In this study, we investigated the potential for observation of virtual hand movements within a P300-based BCI as a feedback system to activate the mirror neuron system. We also explored the role of feedback anticipation and estimation mechanisms during movement observation. Twenty healthy subjects participated in the study. We analyzed event-related desynchronization and synchronization (ERD/S) of sensorimotor EEG rhythms and Error-related potentials (ErrPs) during observation of virtual hand finger flexion presented as feedback in the P300-BCI loop and compared the dynamics of ERD/S and ErrPs during observation of correct feedback and errors. We also analyzed these EEG markers during passive AO under two conditions: when subjects anticipated the action demonstration and when the action was unexpected. A pre-action mu-ERD was found both before passive AO and during action anticipation within the BCI loop. Furthermore, a significant increase in beta-ERS was found during AO within incorrect BCI feedback trials. We suggest that the BCI feedback may exaggerate the passive-AO effect, as it engages feedback anticipation and estimation mechanisms as well as movement error monitoring simultaneously. The results of this study provide insights into the potential of P300-BCI with AO-feedback as a tool for neurorehabilitation

Controlling actions and experiencing control: the influence of movement execution and goal achievement on the Sense of Agency

Some recent theoretical models of the Sense of Agency - i.e., the feeling of controlling one's movements and their impact on the external environment (Aarts et al., 2012; Moore & Fletcher, 2012; Tsakiris et al., 2010) - suggest that this experience relies on the integration of various cues (Synofzik, 2008; Moore & Fletcher, 2012). However, only a few studies (Caspar, et al., 2016; David et al., 2016) manipulated in the same paradigm information about the executed movement and information about the achievement of the goal of the action. Hence, the respective roles of these two action cues for the Sense of Agency remains unclear. My Ph.D. thesis presents the results of two studies aimed at filling this gap. During my Ph.D., my colleagues and I devised a novel paradigm where participants performed a simple goal-directed action – pressing a button of a certain color – while they observed a virtual hand performing an action in a virtual scenario from a first-person perspective. The virtual action could be similar or different with respect to the one executed by the participant, and information about movement and about the achievement of the goal of the action could be independently and simultaneously manipulated. While participants performed the task, we collected direct and indirect measures of their Sense of Agency. In addition, we measured participant’s reaction times: indeed, a second aim of these two studies was to understand whether unexpected movement and goal related information also affects participant’s behavior and leads to behavioral adjustments, similarly to the commission of real errors (Danielmeier & Ullsperger, 2011). A detailed description of the paradigm, and the results of two behavioral studies where we employed it are reported in the thesis. In chapter 1, I provide an overview of literature supporting the fact that the Sense of Agency is sensitive both to the control of one's movements and to the achievement of the goal of the action. However, I also show that these two action cues were mostly investigated separately, which prevents a comparison of their relevance for the Sense of Agency. In chapter 2 I present the result of the first study. Our aim was to understand how violated predictions concerning movement execution and the achievement of the goal of the action influence the Sense of Agency. In Chapter 3, I present the results of the second study, where we compared the effects of the manipulation of information relative to movement execution and goal achievement respectively in freely chosen and cued actions. In particular, we wanted to investigate the influence of freedom to act on the Sense of Agency. Finally, in the Appendix I report preliminary results of an experiment where we investigated the neurocognitive processes (by means of Transcranial Magnetic Stimulation) underlying a different but related topic: the capacity of the individuals to exert agency, i.e., to control one’s own ocular movements when one is exposed to potentially distracting social stimuli (i.e., other’s gaze). Overall, the results of the studies described in chapters 2 and 3 suggest that the Sense of Agency is mostly influenced by movement related information, and that under some specific circumstances the feeling of control is also influenced by goal achievement and by freedom to act. Additionally, unexpected information concerning both the executed movement and the achievement of the goal of the action may lead to behavioral adjustments

Psychophysiological Biomarkers of Concussion Recovery

Each ach year a growing number of individuals report lingering deficits months-years following concussion. Persistent post-concussion symptoms (PPCS) can negatively impact day-today activities and if left untreated may manifest in severe neurological sequelae resulting in long-term cognitive impairment or advanced neurological degeneration (i.e., CTE). Current clinical diagnostic and prognostic assessments (e.g., symptom reports and neurocognitive testing) lack the sensitivity to quantify neurological function. Accordingly, there is a critical need to identify objective biomarkers specific to PPCS to improve an individual’s quality of life and prevent severe long-term neurological dysfunction. Psychophysiological measurements (e.g., EEG derived event-related potentials, heart rate variability, and indices of pupil dynamics) utilize involuntary fluctuations in organ behavior (brain potentials, heart rate, pupil size) in response to environmental events quantify higher-order neurological function. Numerous studies have indicated significant alterations in psychophysiological function in both acute (days-weeks) and chronic (months-years) phases of concussion recovery. These studies demonstrate that psychophysiological measures may possess the necessary sensitivity to serve as reliablemeasures of concussion recovery. However, previous methodological limitations have restricted cross study comparisons and implementation into clinical settings. Specifically, few research studies directly compare currently asymptomatic and symptomatic individuals with a recent history of concussion. This comparison is critical as previous research has demonstrated neurological deficits months to years following injury. By excluding this comparison analytical interpretations fail to account for neurological adaptations that may underlie typical recovery patterns. Additionally, traditional psychophysiological assessments employ task paradigms that do not fully capture the complexity of real-world engagement. If a task is too simplistic, it may fail to adequately challenge the individual and may not reveal lingering neurological dysfunction when completing tasks in the real-world. The present series of investigations found demonstrated that symptomatic individuals with a history of concussion report significant symptom burden spanning somatic disruptions, psycho-affective health, and general quality of life. Furthermore, symptomatic individuals demonstrated significant deficits in tasks of cognitive control, executive function, and attention. These deficits were exacerbated by more complex tasks designed to mimic real-world interactions. In addition to behavioral deficits, both symptomatic and asymptomatic individuals tended to demonstrate lingering deficits in psychophysiological function (i.e., pupillometry and ERPs). Unfortunately, ERP measures collected during more dynamic and complex tasks produced muted waveforms making comparisons across groups difficult. Finally, deficits in both cognitive performance and psychophysiological behavior demonstrated significant relationships with reported symptom burden. This supports their use as potential biomarkers of neurological dysfunction following concussion. In conclusion, the present series of studies supports the growing body of literature suggesting slow-to-recovery demonstrate lingering impairments in neurological function. Furthermore, behavioral assessments designed to mimic real-world interactions may more precisely capture day-to-day impairments. However, these tasks may be too complex and therefore distort neuroelectric recordings of cognitive functio