Midcingulate Motor Map and Feedback Detection: Converging Data from Humans and Monkeys

Abstract

The functional and anatomical organization of the cingulate cortex across primate species is the subject of considerable and often confusing debate. The functions attributed to the midcingulate cortex (MCC) embrace, among others, feedback processing, pain, salience, action-reward association, premotor functions, and conflict monitoring. This multiplicity of functional concepts suggests either unresolved separation of functional contributions or integration and convergence. We here provide evidence from recent experiments in humans and from a meta-analysis of monkey data that MCC feedback-related activity is generated in the rostral cingulate premotor area by specific body maps directly related to the modality of feedback. As such, we argue for an embodied mechanism for adaptation and exploration in MCC. We propose arguments and precise tools to resolve the origins of performance monitoring signals in the medial frontal cortex, and to progress on issues regarding homology between human and nonhuman primate cingulate cortex.

Prefrontal Markers and Cognitive Performance Are Dissociated during Progressive Dopamine Lesion

“…We and others have previously reported this marker in monkeys [8] and humans [5]. It is thought to arise from a source in the MCC [11] and to be sensitive to dopaminergic modulations [8,10]. …”

“…We can, however, draw only limited conclusions from the PET data set with respect to direct PFC and MCC physiology, due to the low levels of DAT in those regions [55,56]. Binding of DAT in lateral prefrontal cortex was indeed negligible, but S4 Fig shows binding potential of the anterior cingulate region of interest (ROI) (derived from [57]), which includes the region we refer to as MCC [11], as well as for caudate and putamen ROIs. Binding potential in this cingulate ROI is much lower than the striatum, but as in our previous study, DAT binding in cingulate was the highest across all cortical regions, and there is support from immunohistochemical localisation for DAT in this region [56].…”

“…These performance-monitoring signals are in many cases generated in midcingulate cortex (MCC [10,11]). These signals appear to provide information about the value of the feedback in terms of behavioural adaptation [12,13], be it for directly driving adaptation on subsequent trials [14] or for motivating more extended behaviours beyond simple trial-to-trial adaptation [15–17].…”

A unilateral medial frontal cortical lesion impairs trial and error learning without visual control

“…Appropriate performance in the PST requires the ability to integrate the successive actions and feedback to adapt behaviour properly after errors and after discovery of the correct response 14 2006; Quilodran et al, 2008). Several sources of correlative evidence in monkeys and humans suggest that action-feedback contingency processing involves maps in MCC (Procyk et al, 2014). In human fMRI, juice feedback responses co-localize with voluntary tongue motor control to the CMAr (Amiez et al, 2013).…”

“…Indeed, we recently provided evidence that in the MCC, and specifically the cingulate motor areas (CMAs), there is a conjunction of the processing of motor act and feedback within particular motor domains (Procyk et al, 2014), such that processing of the feedback can be said to be embodied. Based on this research, we hypothesized that processing in the MCC and pre-SMA is necessary to bind together motor action and the resultant feedback in exploratory situations when adapting of behaviour is required.…”