Abstract
Action update, substituting a prepotent behavior with a new action, allows the organism to counteract surprising environmental demands. However, action update fails when the organism is uncertain about when to release the substituting behavior, when it faces temporal uncertainty. Predictive coding states that accurate perception demands minimization of precise prediction errors. Activity of the right anterior insula (rAI) is associated with temporal uncertainty. Therefore, we hypothesize that temporal uncertainty during action update would cause the AI to decrease the sensitivity to ascending prediction errors. Moreover, action update requires response inhibition which recruits the frontostriatal indirect pathway associated with motor control. Therefore, we also hypothesize that temporal estimation errors modulate frontostriatal connections. To test these hypotheses, we collected fMRI data when participants performed an action-update paradigm within the context of temporal estimation. We fit dynamic causal models to the imaging data. Competing models comprised the inferior occipital gyrus (IOG), right supramarginal gyrus (rSMG), rAI, right presupplementary motor area (rPreSMA), and the right striatum (rSTR). The winning model showed that temporal uncertainty drove activity into the rAI and decreased insular sensitivity to ascending prediction errors, as shown by weak connectivity strength of rSMG→rAI connections. Moreover, temporal estimation errors weakened rPreSMA→rSTR connections and also modulated rAI→rSTR connections, causing the disruption of action update. Results provide information about the neurophysiological implementation of the so-called horse-race model of action control. We suggest that, contrary to what might be believed, unsuccessful action update could be a homeostatic process that represents a Bayes optimal encoding of uncertainty.
Highlights
Action update, the ability to replace an ongoing behavior with a new action, enables us to navigate a volatile environment
We tested the hypotheses that when participants perform action update within the context of temporal estimation, uncertainty induced by temporal gaps affects the right anterior insula (rAI) sensitivity to ascending prediction errors, and time estimation error (TEE) modulate corticostriatal connections
The dynamic causal modeling (DCM) analysis showed that temporal gaps influence the rAI, and
Summary
The ability to replace an ongoing behavior with a new action, enables us to navigate a volatile environment. Unlike the rPreSMA, the rAI is strongly associated with both unsuccessful response inhibition (Cai et al, 2014) and uncertainty (Volz et al, 2003; Hsu et al, 2005; Grinband et al, 2006; Platt and Huettel, 2008; Schultz et al, 2008; Sarinopoulos et al, 2010; Mushtaq et al, 2011; Venkatraman and Huettel, 2012; Grupe and Nitschke, 2013; Limongi et al, 2013; Payzan-Lenestour et al, 2013; Yoshida et al, 2013; Ghahremani et al, 2015) These empirical works suggest that the rAI plays a central role when temporal uncertainty and TEEs induce unsuccessful action update. We used DCM to test for driving and modulatory effects of temporal uncertainty and TEEs on the rAI activity and frontostriatal connections associated with the indirect pathway
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