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

Emmanuel Procyk,Charles R E Wilson,Michael Petrides,Céline Amiez,Frederic M Stoll,Maïlys C M Faraut

doi:10.1093/cercor/bhu213

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.

Highlights

Primates show a remarkable ability to adapt in the face of rapidly changing environments
The single-subject data reported on individual morphology for hemispheres with and without a paracingulate sulcus, and in relation to the extent of the 3 cingulate motor zones as described by Amiez and Petrides (2014) reveal that both activations for juice feedback in exploration and for tongue movements are located in RCZa and are associated with the paracingulate sulcus when this sulcus is present
We further argue that feedback processing in general is embodied in the rostral cingulate motor area (CMAr) which is a specialized area of the midcingulate cortex (MCC) that may have evolved for higher control of motor action and decision making in both species

Summary

Introduction

Primates show a remarkable ability to adapt in the face of rapidly changing environments. In the search for MCC functions, discrepancies between human and monkey studies, and between functional and lesion data (Fellows and Farah 2005; di Pellegrino et al 2007; Nachev 2011), have fueled debates on the exact contribution of this subdivision and, to some extent, on the validity of the nonhuman primate as a model of human cingulate functions (Cole et al 2009; Schall and Emeric 2010). We perform a meta-analysis of cingulate feedback-related unit activity in monkey to show a functional homology with human anterior MCC. This approach allows us to discuss a possible functional organization principle in MCC, and to provide testable hypotheses

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