Conscious perception of errors and its relation to the anterior insula

Abstract

To detect erroneous action outcomes is necessary for flexible adjustments and therefore a prerequisite of adaptive, goal-directed behavior. While performance monitoring has been studied intensively over two decades and a vast amount of knowledge on its functional neuroanatomy has been gathered, much less is known about conscious error perception, often referred to as error awareness. Here, we review and discuss the conditions under which error awareness occurs, its neural correlates and underlying functional neuroanatomy. We focus specifically on the anterior insula, which has been shown to be (a) reliably activated during performance monitoring and (b) modulated by error awareness. Anterior insular activity appears to be closely related to autonomic responses associated with consciously perceived errors, although the causality and directions of these relationships still needs to be unraveled. We discuss the role of the anterior insula in generating versus perceiving autonomic responses and as a key player in balancing effortful task-related and resting-state activity. We suggest that errors elicit reactions highly reminiscent of an orienting response and may thus induce the autonomic arousal needed to recruit the required mental and physical resources. We discuss the role of norepinephrine activity in eliciting sufficiently strong central and autonomic nervous responses enabling the necessary adaptation as well as conscious error perception.

Fig. 1

Correlation of error positivity (Pe) and P3b, suggestive of a common functional significance in terms of orienting to salient events (adapted from Ridderinkhof et al. 2009). In an oddball task, infrequent target stimuli trigger an orienting response reflected in the P3b. The orienting response is most evident in the effect of the interval between successive targets (expressed in terms of the number of intermittent nontargets) on P3b amplitude. Individual differences in this effect of target–target–interval (TTI) on the P3b amplitude were found to co-vary (r = 0.47) with individual differences in the amplitude of the Pe obtained from erroneous responses in a Simon task

Fig. 2

Results of metaanalysis performed separately for pre-response conflict (PRC), decision uncertainty (DU), response errors (RE), and negative feedback (NF), projected on coronal, right sagittal, and axial slices. Alpha level = 0.01. L/R left/right, pMFC posterior medial frontal cortex

Fig. 3

Schematic of timing and interaction of processes during an erroneous trial that may support error awareness. a Timing of external and internal events as well as psychophysiological measures associated with the accumulation of evidence that the response was erroneous (not to scale). The latency of conscious error perception may vary substantially and should result from accumulation of sufficient evidence that an error has occurred, independent of the source of information which may range from early pMFC-mediated error monitoring via proprioceptive and sensory input discordant with expectancies from forward modeling to interoception. The numbered arrows indicate different influences that may lead to error blindness: 1 ambiguous stimuli make it objectively impossible to detect errors. Also fluctuations in attention or eye blinks precluding the perception of short stimuli may result in errors that cannot be detected reliably. 2 failure to represent task sets or to activate complex task rules may lead to errors. 3 insufficient efference copy, proprioceptive feedback or sensory input on action effects may hinder conscious perception of an error. 4 interactions with ongoing fluctuations in brain activity may lower signal-to-noise ratio in the representation of accumulating evidence of erroneous behavior. Moreover, action slips in the signaling or accuracy classification response may occur. b Influence of accumulating evidence of an error on different processes and correlates during error monitoring. It is unclear whether processes are working in serial or—at least partly—parallel fashion and how much they depend on each other. In particular the causal relationship of error awareness, some post-error adjustments and autonomic responses is still unclear

Fig. 4

Pupil diameter just prior to errors predicts opposing neural network dynamics that are supported by changes in functional connectivity of anterior insular cortex (AIC), but only when subjects become aware of the error (adapted from Harsay et al. 2010). Preparatory pupil diameter predicts increased activation of AIC and salience/control structures (RCZ rostral cingulate zone, S primary sensory cortex, and task control oculomotor structures IPS intraparietal sulcus, FEF frontal eye field) and decreased activation in the default mode network (aMPFC anterior medial prefrontal cortex, and PCC posterior cingulate cortex). Likewise, preparatory pupil diameter predicts functional connectivity of AIC with nodes of the attention/control networks (S, IPS) increased at the expense of functional connectivity with nodes of the default mode network (aMPFC)