Temporal Uncertainty and Temporal Estimation Errors Affect Insular Activity and the Frontostriatal Indirect Pathway during Action Update: A Predictive Coding Study

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.

Temporal Prediction Errors Affect Short-Term Memory Scanning Response Time

“…The mean proportion of correct responses shows that participants performed the task as instructed, M = 0.83, SD = 0.37, 95% CI [0.82, 0.84]. The linear mixed-effects model shows that absolute temporal PEs increased linearly as a function of the temporal gap (β = 0.18, SE = 0.006, t (4,304) = 31.41, p < .001), which replicates previous results (Limongi et al, 2013, 2015, 2016; Young et al, 2005).…”

“…Specifically, the disruptive effect of PEs on response reengagement has been thought to be mediated by a decrease in the precision of the information that the frontal cortex sends to the striatum. The decreased precision might be reflected in weak frontostriatal connections (Limongi et al, 2015, 2016). In different words, influences exerted by frontal areas on striatal regions would be weaker in the context of large temporal PEs.…”

Successful and unsuccessful response inhibitions differentially affect the effective connectivity between insular, presupplementary-motor, and striatal areas.

“…Absolute TEEs provide a better interpretation of the effects of implicit time estimation on temporal prediction. This has been previously demonstrated at a behavioral and neurophysiological levels (Limongi et al, 2016;Limongi et al, 2015;Limongi et al, 2013;Young, Rogers, & Beckmann, 2005). At a behavioral level, absolute values allow to differentiate the effects that produce the same mean TEE but different dispersions (Young et al, 2005).…”

Glutamate and Dysconnection in the Salience Network: Neurochemical, Effective-connectivity, and Computational Evidence in Schizophrenia

“…On the F-contrast, a sphere (8-mm radius) was centered on the Montreal Neurological Institute coordinates corresponding to the dACC (the same coordinates that formed the centroid of the 1 H-MRS voxel for the [Glu]dACC measurements) and to the AI (X = 38, Y = 20, Z = -4, Fig. 1) -we selected these coordinates based on our previous results (37).…”