Functional heterogeneity of conflict, error, task-switching, and unexpectedness effects within medial prefrontal cortex

Abstract

The last decade has seen considerable discussion regarding a theoretical account of medial prefrontal cortex (mPFC) function with particular focus on the anterior cingulate cortex. The proposed theories have included conflict detection, error likelihood prediction, volatility monitoring, and several distinct theories of error detection. Arguments for and against particular theories often treat mPFC as functionally homogeneous, or at least nearly so, despite some evidence for distinct functional subregions. Here we used functional magnetic resonance imaging (fMRI) to simultaneously contrast multiple effects of error, conflict, and task-switching that have been individually construed in support of various theories. We found overlapping yet functionally distinct subregions of mPFC, with activations related to dominant error, conflict, and task-switching effects successively found along a rostral-ventral to caudal-dorsal gradient within medial prefrontal cortex. Activations in the rostral cingulate zone (RCZ) were strongly correlated with the unexpectedness of outcomes suggesting a role in outcome prediction and preparing control systems to deal with anticipated outcomes. The results as a whole support a resolution of some ongoing debates in that distinct theories may each pertain to corresponding distinct yet overlapping subregions of mPFC.

Figure 1

A) Plot of 110 peaks from 43 studies examining response conflict (adapted from (Nee et al., 2007). Clustering is evident in RCZp, as well as the pre-SMA. B) Zones corresponding to RCZa (red), RCZp (green), and the pre-SMA (cyan) as described by Picard and Strick (2001). VAC – vertical anterior commissure line.

Figure 2

Depiction of the task design. Subject's were presented with a face overlaid with a body part (limb) and responded to the species of the relevant task (face or part). The relevant task was not explicitly cued and had to be derived from feedback. A) The face and body part are of the same species (human) producing a Congruent trial. The subject responds appropriately and receives positive feedback (+1000). B) The face and body part are of different species and the subject is on the correct task (face) and responds appropriately (human). C) The subject responds inappropriately on a Congruent trial. D) The subject is on the face task but the task has changed to part, unbeknownst to the subject. Upon receiving negative feedback the subject now must switch tasks.

Figure 3

Whole-brain results from each contrast of interest. Each contrast produces a similar pattern of lateral frontal, medial frontal, and lateral posterior parietal activations. Switch-related activations (middle) produced activations in more dorsal portions of mPFC that were not found in the Conflict contrast (top). Error-related activations in mPFC (bottom) extended more inferiorly and anteriorly.

Figure 4

A) Contrast of Task-Switching and Conflict contrasts. Differences were found throughout much of the mPFC and strongest in dorsal aspects including RCZp and the pre-SMA. B) Contrast of Error and Task-Switch trials. Differences were largely restricted to the cingulate gyrus adjacent to the corpus callosum in Brodmann's Area 24.

Figure 5

Activations by position in the mPFC. First, an ROI was defined that combined Conflict, Task-Switching, and Error-related activations. Next, this ROI was sliced horizontally through the z-plane (A, left) and vertically through the y-plane (B, left). Within each slice, the average t-statistic was computed separately for Conflict (blue), Switching (green), and Error (red) contrasts. In ventral and anterior regions of the mPFC ROI, Error-related activation dominated. In dorsal and posterior regions, Errors and Switching were equivalent. Conflict-related activation was less strong than both Switching and Error-related activation throughout.

Figure 6

Bottom Left : Spherical ROIs were placed into 4 sub-regions based upon the averaged anatomical image of the subjects in this study and demarcations suggest by Picard and Strick (2001). Vertical lines are drawn through the tip of the genu of the corpus callosum and through the anterior commisure, with the curved lines outlining RCZ between these landmarks. Spheres were placed in the cingulate gyrus anterior to the genu (blue), RCZa (red), RCZp (green), and pre-SMA (cyan) dorsal to RCZ and anterior to the anterior commisure. Top left: Conflict, Switching, and Error contrasts as a function of region. Top right: A comparison of Switching and Conflict contrasts by region. Bottom right: A direct contrast of Error and Switch trials (see Methods).

Figure 7

Finite impulse responses (FIRs) demonstrating the time-courses of the hemodynamic response in RCZa and RCZp. Whereas hemodynamic responses to errors and task-switches were similar in the two regions, incongruent trials produced deactivations in RCZa and activations in RCZp.

Figure 8

Congruency × Accuracy interactions in RCZp. Top Left: Time courses of activation in RCZp for correct congruent, correct incongruent, incorrect congruent, and incorrect incongruent trials. Top Right: RCZp demonstrated a conflict (incongruent, congruent) × error (correct, error) interaction. Bottom Left: Error rates measured behaviorally correlated negatively with the Error neural contrast. Bottom Right: RT measurements of conflict correlated positively with the Conflict neural contrast.

Figure 9

A) Activation in RCZp as a function of the log-probability of outcomes (correct | congruent; error | congruent; correct | incongruent; error | incongruent; switch | incongruent). B) whole-brain exploratory correlations with log-probability of outcomes demonstrated foci in RCZa, RCZp, and the insula. C) Correlations between activations in CG, RCZa, RCZp, and preSMA and log-probability of outcomes.