Connectional gradients underlie functional transitions in monkey pre-supplementary motor area

Davide Albertini,Marzio Gerbella,Marco Lanzilotto,Alessandro Livi,Monica Maranesi,Carolina Giulia Ferroni,Luca Bonini

doi:10.1016/j.pneurobio.2019.101699

Davide Albertini, Marzio Gerbella + Show 5 more

Open Access

https://doi.org/10.1016/j.pneurobio.2019.101699

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Abstract

The pre-supplementary motor area F6 is involved in a variety of functions in multiple domains, from planning/withholding goal-directed actions in space to rule-based cognitive processes and social interactions. Yet, the neural machinery underlying this functional heterogeneity remains unclear. Here, we measured local population dynamics in different rostro-caudal sites of cytoarchitectonically verified area F6 in two monkeys during spatial, contextual and motor processes, both in individual and social conditions. Then, we correlated multimodal population tuning with local anatomical connectivity revealed by neural tracer injections into the functionally characterized sites. We found stronger tuning for object position relative to the monkey in the rostral portion of area F6 than in its caudal part, which in turn exhibits stronger tuning to self and other’s (observed) action. Functional specificities were associated with a rostro-caudal transition in connectivity strength from lateral prefrontal cortex, pregenual anterior cingulate cortex and associative striatum (rostrally), to dorso-ventral premotor areas and the motor putamen (caudally). These findings suggest that the functional heterogeneity of the pre-supplementary area F6 is accounted for by gradual transitions in functional properties grounded on local cortico-cortical and cortico-striatal connectional specificities.

Highlights

The pre-supplementary motor area lies in the mesial wall of the cerebral hemispheres, rostrally to the supplementary motor area (Matsuzaka et al, 1992; Picard and Strick, 1996)
Recent studies indicate that F6 plays a role in social behavior and is part of a brain network dedicated to the processing of social interactions (Sliwa and Freiwald, 2017)
Neuronal activity was recorded from four cortical sites at distinct rostro-caudal positions along area F6 of the two monkeys (Fig. 1C), spanning the entire extent of the cytoarchitectonically verified area F6

Summary

Introduction

The pre-supplementary motor area (called F6 in the monkey, see Matelli et al, 1991; Luppino et al, 1991) lies in the mesial wall of the cerebral hemispheres, rostrally to the supplementary motor area (Matsuzaka et al, 1992; Picard and Strick, 1996). It receives inputs from prefrontal and cingulate cortex and sends projections to parietodependent areas of the dorsal and ventral premotor cortex (Rizzolatti and Luppino, 2001; Johansen-Berg et al, 2004; Morecraft et al, 2012), being optimally placed for “linking cognition to action” (Nachev et al, 2008), and to act as a hub for processes related with motor intentionality (Zapparoli et al, 2018). Two main hypotheses have been proposed concerning its anatomo-functional organization: 1) F6 is a unitary, essentially homogeneous, anatomo-functional area (e.g. (Rizzolatti and Luppino, 2001)), which underlies a specific but still unclear functional signature, or 2) it indexes a variety of functional properties linked with gradual rostro-caudal transitions in local connectional specificities (Nachev et al, 2008)

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