New insights into neural networks of error monitoring and clinical implications: a systematic review of ERP studies in neurological diseases

Abstract

Error monitoring allows for the efficient performance of goal-directed behaviors and successful learning. Furthermore, error monitoring as a metacognitive ability may play a crucial role for neuropsychological interventions, such as rehabilitation. In the past decades, research has suggested two electrophysiological markers for error monitoring: the error-related negativity (ERN) and the error positivity (Pe), thought to reflect, respectively, error detection and error awareness. Studies on several neurological diseases have investigated the alteration of the ERN and the Pe, but these findings have not been summarized. Accordingly, a systematic review was conducted to understand what neurological conditions present alterations of error monitoring event-related potentials and their relation with clinical measures. Overall, ERN tended to be reduced in most neurological conditions while results related to Pe integrity are less clear. ERN and Pe were found to be associated with several measures of clinical severity. Additionally, we explored the contribution of different brain structures to neural networks underlying error monitoring, further elaborating on the domain-specificity of error processing and clinical implications of findings. In conclusion, electrophysiological signatures of error monitoring could be reliable measures of neurological dysfunction and a robust tool in neuropsychological rehabilitation.

Selective influence of dopamine on electrocortical signatures of error monitoring: a combined EEG and immersive virtual reality study in Parkinson’s disease

“…This evidence is in line with findings in other clinical populations, such as patients with ACC lesion (Maier et al, 2015; for systematic reviews see Lenzoni et al, 2021 andPezzetta et al, 2021) in which the Pebut not the ERN/theta -was unaltered. It was previously found that patients with lateral prefrontal lesion which extended to the insula had reduced Pe response (Ullsperger et al, 2002;Ullsperger & von Cramon, 2006), suggesting that the activity associated to the Pe activity might engage a neural network involving not only the ACC, but also anterior insula and somatosensory areas (Ullsperger et al, 2010), that may be spared in PD.…”

“…From a neuroanatomical and functional point of view, mounting evidence suggest that the prefrontal cortex, including the dorsal ACC generates error-related midfrontal theta/ERN as a low-level mismatch between the actual and expected response (Cavanagh et al, 2014; Jocham & Ullsperger, 2009; Parker et al, 2005; Ridderinkhof et al, 2004b). On the other hand, less clear is the origin of the Pe, which has been associated with the engagement of different areas such as the anterior parts of the ACC (Holroyd & Coles, 2002), posterior portions of the cingulate (Vocat et al, 2008) and insular cortices (Klein et al, 2013), which in turn have been associated to the salience network (Lenzoni et al, 2021; Orr et al, 2011; Wessel, 2017); the Pe/oPe seem to signal the awareness of an error, following motivational and affective events, and may be link with post-error adaptation (Overbeek et al, 2005; Danielmeier & Ullsperger, 2011). The distinct cortical involvement of these error-related responses is in line with evidence suggesting the existence of independent mechanisms underlying the error monitoring system (di Gregorio et al, 2018; Steinhauser & Yeung, 2010), that seem also to rely on distinct neurotransmitters (Falkenstein et al, 2005; Holroyd & Coles, 2002).…”

“…In this vein, testing PD patients while under their dopaminergic medication (‘on-condition’) and after dopaminergic withdrawal (‘off-condition’) can be an ideal model for exploring the selective influence of dopamine on different EEG correlates of error monitoring. Few EEG studies reported diminished amplitude of the ERN/theta during action execution in PD, while some other studies found mixed results for the Pe (see Lenzoni et al, 2021 and Pezzetta et al, 2021 for systematic reviews). It is worth noting that only two studies used the time-frequency approach (Beste et al, 2017; Singh et al, 2018) and only one found no difference due to dopaminergic medication in conflict-related theta (Singh et al, 2018).…”

Effects of psychological fatigue on college athletes’ error-related negativity based on artificial intelligence computing method

“…Researchers believed that ERN combined with Pe can deepen the understanding of ERN understanding [3]. Some scholars have presented both ERN and Pe in their research results [29,30]. ERN had been proposed to reflect early performance monitoring and error detection, while Pe had been connected to subsequent error awareness [31].…”

Self-awareness in Dementia: a Taxonomy of Processes, Overview of Findings, and Integrative Framework

“…Similarly, self-awareness manifest through metacognition is not exclusively a higher-order process, since it involves early 'preconscious' representations, apparent for example in electrophysiological signatures of error-monitoring, such as the early error-related negativity (ERN) and subsequent error positivity (Pe), which can be selectively compromised in neurological disorders [48]. Homologous mechanisms are shown to operate also in non-human primates [49], and, in humans, the Pe is associated with both awareness of error and accompanying psychophysiological responses [50].…”