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.

Keywords: decision; learning; prefrontal; primate; reward.

Figure 1.

Schematic representations of the ACC and MCC region in the human (A,B) and macaque (C) brains according to Vogt et al. Overlap on brain anatomical scans average in MNI standard spaces for both species. The regions ACC, MCC, PCC, and RSC are based on the 4 regions subdivision by Vogt et al. (Vogt et al. 2005; Palomero-Gallagher et al. 2009; Vogt 2009b). The human representations schematize the organization of cingulate subdivisions in the case of absence (A) or presence (B) of the paracingulate sulcus. Area 32′ and a24c′ were defined by the same authors. In A, the schematic limits of anterior and posterior MCC (aMCC and pMCC) are shown. In C, the schematic position of cingulate motor areas (CMAr, CMAd, CMAv) are presented as in He et al. (1995).

Figure 2.

Human cingulate motor areas, feedback activity, and sulcal morphology. (A) Schematic illustration of the 3 human cingulate motor areas (RCZa, RCZp, and CCZ) as described by Amiez and Petrides (2014). Colored disks represent the average location of activation peaks in response to simple voluntary movements for hemispheres with (top) and without (bottom) a paracingulate sulcus. cs: cingulate sulcus, pcs: paracingulate sulcus. (B) Overlap of tongue movement-related activation peaks (individual peak locations are represented by squares) and peaks for feedback-related activation (circles) during exploration for hemispheres with and without a paracingulate sulcus. Each individual sulcus path has been retraced, and all paracingulate (blue) and cingulate (yellow) sulci, as well as vertical branches (red, green, and white), have been overlapped for the populations of subjects. Data taken from Amiez et al. (2013) and Amiez and Petrides (2014). Note, the activation data come from 2 separate experiments. The approximate location of RCZa, RCZp, and CCZ is indicated by ellipses (rostrocaudal extent estimated from Amiez and Petrides 2014).

Figure 3.

Database for meta-analysis in monkeys. Rostrocaudal extent of (top) recording sites in studies reporting feedback/outcome-related activity, (middle) regions with face-related effects of microstimulations and regions with anatomical connections with face-related areas and nuclei, and (bottom) regions with arm-related effects of microstimulations and regions with connections with arm-related areas and spinal levels. On the left of recording sites extent, symbols of an eye and of a hand indicate the effector used by animals to respond. On the left of Eye/Face studies, “e” and “f” relate to studies focusing on eye-related data (e.g., connections to FEE) or to face-related data (e.g., connection to M1 face), respectively. The specificity of anatomical studies is indicated in brackets (FEF, SEF, M1, C4-T2, C2-C4, C7-T1: injections of tracer in the respective cortical or spinal regions; mstim: microstimulation study; 2DG: study using 2-deoxyglucose). All data are aligned to the level of the genu of the arcuate sulcus (anterior 0, ArcGen). See Supplementary Information for details.

Figure 4.

Meta-analysis of functional and anatomical data in monkeys. (A) Number of studies covering the rostrocaudal regions of the dorsal bank of the cingulate sulcus (data from Fig. 3). Single-unit recording studies are represented in the opened sulcus. Eye/face data and forelimb-related data are shown just below. Red in the color scale indicates a greater number of studies. AP coordinates for genu of the arcuate (genArc), caudal end of principalis (endSP), and genu of the Corpus Callosum (genCC) are averages taken from a population of 11 rhesus monkeys (from MRI images). (B) Histogram of data reported along the cingulate sulcus for recordings related to outcome/feedback (yellow), and for anatomical maps for Eye/Face representation (orange) and Forelimb (purple). Comparing distributions reveals that data for Eye/Face and outcome/feedback are different in terms of antero-posterior coverage at P < 0.01, but that both differ from the distribution related to Forelimb at P < 10⁻⁸. The rostrocaudal extent is aligned on ArcGen. (C) Schematic overlap of eye/face-related data reconstructed from 7 studies. Maps are aligned on the rostrocaudal level of the genu of the arcuate sulcus (ArcGen).