Error Monitoring Using External Feedback: Specific Roles of the Habenular Complex, the Reward System, and the Cingulate Motor Area Revealed by Functional Magnetic Resonance Imaging

Abstract

The dopaminergic system has been shown to be involved in the processing of rewarding stimuli, specifically of errors in reward prediction, in animal studies as well as in recent neuroimaging studies in humans. Furthermore, a specific role of dopamine in the human homolog of the rostral cingulate motor area (rCMA) was proposed in a recent model of error detection. Negative feedback as well as self-detected errors elicit a negative event-related brain potential probably generated in the rCMA. We performed two experiments using functional magnetic resonance imaging to investigate the brain activity related to negative and positive feedback in a dynamically adaptive motion prediction task. Whereas positive feedback raised hemodynamic activity in the ventral striatum (nucleus accumbens), negative feedback activated the rCMA, the inferior anterior insula, and the epithalamus (habenular complex). These data demonstrate the role of the habenular complex in the control of the human reward system, a function previously hypothesized on the basis of animal research. The rCMA reacted only to errors with negative feedback but not to errors without feedback, which ruled out an influence of response conflict or uncertainty on its role in error detection by external signals.

Neural dynamics of error processing in medial frontal cortex

“…4). These results show not only that the anterior cingulate cortex responds to both internal (Carter et al, 1998;Garavan et al, 2002;Ullsperger and Von Cramon, 2001) and external (Holroyd et al, 2004b;Ullsperger and Von Cramon, 2003) sources of error information, but also that this cingulate region responds to the earliest source of error information available.…”

“…In this paper, we focus our analysis on the rostral cingulate zone anterior (RCZa), a portion of the anterior cingulate cortex which has previously been associated with response errors (Ullsperger and Von Cramon, 2001), negative feedback (Ullsperger and Von Cramon, 2003), and reductions in reward leading to behavioral adjustments (Bush et al, 2002). This area is suggested to correspond to the monkey rostral cingulate motor area (Picard and Strick, 1996) and is situated in what Bush et al (2000) described as the Fcognitive_ division of the anterior cingulate cortex.…”

Errors recruit both cognitive and emotional monitoring systems: Simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI

“…6AB, the slow hits (but not errors and fast hits) showed a highly significant correlation (Pearsons r=.49, p<.001) between the positive peak and actual RT across trials (n=147), indicating that slower RTs were associated with an earlier positive peak (relative to RT onset). These results suggest a functional coupling between behavioral speed and this positive activity, likely reflecting motor preparation (or execution) taking place in the cingulate motor area (Ullsperger & von Cramon, 2003). Although the early positive activity preceding RTs was inversely related to speed for slow hits (see Fig.…”

“…In this condition, the (peak) latency of the early cingulate positivity was inversely proportional to RT latency (i.e., the earlier this activity peaked relative to RTs, the slower the RTs), suggesting that this region might be closely related to motor preparation stages (see Ullsperger & von Cramon, 2003). This is consistent with the notion that dorsal ACC might receive direct inputs from motor commands in order to monitor ongoing actions or that it might participate to an early stage of motor preparation .…”

Structural and functional hyperconnectivity within the sensorimotor system in xenomelia

“…The nodes with the highest degrees in the 116‐node functional network analyses are located in the middle part of the cingulate cortex bilaterally (10 connections) and in the cerebellum (9 connections). Although we did not formulate any a priori hypothesis with respect to the cingulate cortex, we note that the cingulate motor area, located ventrally adjacent to the SMA, is housed within the middle part of the cingulate cortex (Brazdil, Kuba, & Rektor, 2006; Liberg et al., 2014; Ullsperger & von Cramon, 2003). This cingulate motor area is also part of the sensorimotor system, and it should therefore not come as a surprise that it evidenced an increased functional connectivity in our xenomelia group.…”