Anterior insula activity and the effect of agency on the Stimulus‐Preceding Negativity

Abstract

If you know that you are the author of a freely chosen action and that you bear responsibility for its outcome, then you are said to have “a sense of agency.” When there is a delay between action and outcome, this response must be remembered if you are to learn from the experience. Previous studies have shown that the Stimulus‐Preceding Negativity (SPN) recorded during the delay interval is larger under conditions that foster a sense of agency. In an EEG experiment (N = 27), we confirmed that the SPN is larger when participants have a choice between two responses in a gambling task as compared to when there is only a single button and the computer determines the monetary outcome. This SPN agency effect was largest over right prefrontal cortex and it did not vary significantly between trial blocks in which only gains or only losses were possible. Participants in a second experiment (N = 26) performed the same task while activity in anterior insular cortex, a known SPN generator, was measured via functional magnetic resonance image (fMRI). An essentially identical pattern of results was obtained: Activity was greater on choice than no‐choice trials, especially for the right hemisphere, and no effect of contextual valence was observed. Although parallel observations such as these cannot warrant causal inference, our findings are consistent with the assumption that anterior insular cortex contributes to the effect of agency on the SPN.

As they wait: Anticipatory neural response to evaluative peer feedback varies by pubertal status and social anxiety

“…At the neural level, we observed that adolescents with higher levels of social anxiety displayed heightened SPN activity during social feedback anticipation. This effect was found at the right frontal cluster, which corresponds with prior studies demonstrating frontal dominance of the SPN ( Hackley et al, 2020 ; Kotani et al, 2015 , 2009 ; Masaki et al, 2010 ). We observed that the right frontal SPN was more negative for the anticipation of acceptance versus rejection feedback among adolescents with higher social anxiety symptoms, but this effect was not significant.…”

“…Our sample did not include adults precluding us from directly comparing adults and adolescents and identifying possible developmental differences in the lateralization of the SPN. Although, there are mixed findings regarding localization of the SPN in other tasks, several studies suggest a right preponderance of the SPN which is thought to arise from the right insular reactivity ( Brunia et al, 2011 ; Hackley et al, 2020 ; Kotani et al, 2015 , 2009 ). The effects we found prominently for the right clusters might be, therefore, explained by the lateral localization of the SPN.…”

“…The SPN was calculated by taking the mean amplitude within the 200 ms interval before the feedback presentation (i.e., 2800–3000 ms following the response) at both bilateral frontal and posterior channel clusters (see Supplemental Table S1 and Fig. S1 for reliability and topo plots), considering the mixed findings in the literature regarding the electrode sites where SPN effects were observed (e.g., right anterolateral [F4]; Masaki et al, 2010 ; Hackley et al, 2020 ; frontal [Fz, F1, and F2]; Tanovic and Joormann, 2019 ; left-parietal occipital [PO7]; van der Molen et al, 2014 ). Fig.…”

Learning to deal with delayed outcomes: EEG oscillatory and slow potentials during the prefeedback interval

“…We know from source localization research (Böcker et al, 1994; Catena et al., 2012), including fMRI‐EEG studies (Hackley et al., 2020; Kotani et al., 2015; Seidel et al., 2015; Tsukamoto et al., 2006), that multiple cortical regions contribute to the SPN. To determine if activity within any of these sources reflects hypothetical constructs related to learning (e.g., holding an outcome prediction in mind), it will be necessary to fractionate the SPN into subcomponents.…”

“…When the outcome of an action is delayed by a few seconds, scalp recordings show a frontally distributed negativity, the stimulus‐preceding negativity (SPN), whose amplitude increases with task difficulty (Mattox et al., 2006), with the amount of feedback information (Kotani et al., 2003), and with knowledge regarding feedback veracity (Chwilla & Brunia, 1991). Pertinent to the credit assignment problem is the fact that SPN amplitude is considerably enhanced when the participant has perceived control over the action outcome; in other words, that he or she has a sense of agency (Hackley et al., 2020; Masaki et al., 2010; Mei et al., 2018; Muhlberger et al, 2017). A finding of direct relevance to the current study is that SPN amplitude has been reported to decrease over the course of learning in three very different tasks: perceptual categorization (Morís et al., 2013), cognitive extrapolation (Hirao et al., 2017), and fine motor control (Ren et al., 2017).…”