Alongside the AICs role in performance monitoring, a great deal of evidence has been provided implicating it as a correlate of autonomic nervous system (ANS) activity, ranging from heart beat to indices of pupil diameter (Craig 2002
; Critchley 2005
). It is far from clear, however, what precise association the AIC and the ANS share. Some authors that have reported such associations primarily attribute the role of insular activity to the process of the generation
of autonomic activity, whereas others emphasize a possible key role of the insula in the perception
, rather than the generation, of ANS state and responses. Due to the correlative nature of most neuroimaging techniques, causal ties are hard to establish without the use of patient studies.
As a least common denominator, it seems safe to say, though, that there is a reliable association between the activity of large parts of the ANS and the AIC. As reported earlier, erroneous actions are accompanied by changes in ongoing ANS activity, among reflected in HR, PD, and SCR. Importantly, the response of the ANS is stronger for perceived than for unperceived errors.
Accounts trying to explain the involvement of the ANS in error processing have not always provided clear explanations of the role of the ANS engagement as a consequence of errors. In our aforementioned EEG-ANS study (Wessel et al. 2010
) we interpret our results in the light of recent behavioral experiments (Notebaert et al. 2009
), which suggested strong behavioral parallels between processing of errors and other rare, potentially significant events (e.g., deviant and/or novel stimuli). According to their account, error-related ANS activity is a manifestation of an orienting response (OR, Sokolov 1963
) towards an erroneous outcome. The OR is a reflex-like reaction of the organism to improbable changes in its environment (which are potentially motivationally relevant) and is accompanied by a cascade of CNS and ANS reactions, including HR, PD, and SCR associated with increased arousal. We are aware that the term orienting has been used in many contexts and use it here to indicate the complex arousal response to motivationally salient events rather than orienting attention in space or time. Such OR-related interpretations of error-related ANS activity have been provided already in the 1970s of the twentieth century (Danev and de Winter 1971
), but have not been followed up on in later studies demonstrating ANS activity as a consequence of errors.
The central argument is that an error, much like a rare stimulus, elicits an OR-like reaction. The emergence of an OR towards an infrequent stimulus is heavily dependent on the realization of the potential significance (information content) of the stimulus. For an error to elicit an OR, then, it is reasonable to assume that the emergence of the OR after an error is also associated with its detection. That is, error awareness should be crucial to the emergence of an error-related OR, or vice versa. The larger OR-like ANS activity after perceived errors seems to support this account. Moreover, there are striking parallels between the association of the Pe with error awareness and the association of the P3b with the OR (Ridderinkhof et al. 2009
). Notably, the P3b has been suggested to be related to phasic activity of the LC/NE system (Nieuwenhuis et al. 2005
), as has the OR. The autonomic response to an error may serve to increase autonomic arousal and thus facilitate necessary adjustments. Note that strong responses and associated arousal may also lead to maladaptation. For example, post-error slowing [suggested to be at least in part driven by the OR (Notebaert et al. 2009
)] may be associated with improvements in accuracy (=adaptive) or with decreases in accuracy (=maladaptive) (Rabbitt 1966
; Rabbitt and Rodgers 1977
; Fiehler et al. 2005
). It may be speculated that the adaptiveness of the adjustment depends not only on external factors such as time pressure but also on the pre-trial baseline state of the LC/NE system (see above).
Independently of the arguments as to why the ANS response is different for perceived and unperceived errors, this mere observational fact alone offers a simple possible explanation for the differential effects of error awareness on AIC activity: if the anterior insula serves either as an active agent in eliciting the ANS response, or as a crucial monitor for the milieu interne
(on a proprioceptive/interoceptive level with regard to ANS activity) of the body, the effects of error awareness and error blindness on insular activity might be the same that are responsible for the effects of error awareness on the ANS. As already discussed in Klein et al. (2007
), it is unclear whether (a) AIC activity precedes and causes the ANS response, (b) the ANS response elicits the AIC engagement by interoception, or (c) both occur simultaneously. In other words, it is of great interest whether AIC activity is causal to the ANS activity (and possibly to components of the OR) or whether it serves more for monitoring or interoceptive awareness-related functions. In consequence, it is also of large interest whether the presence of the ANS reaction itself is a mere consequence of error awareness or whether it provides additional input for potential other systems decisive for the conscious recognition of erroneous actions (see Fig. b). This, however, once again underlines the need for lesion studies to establish a causal relationship and its directionality.