Anatomical bases of fast parietal grasp control in humans: A diffusion-MRI tractography study

Nathalie Richard,Michel Desmurget,Achille Teillac,Pierre-Aurélien Beuriat,Lara Bardi,Gino Coudé,Alexandru Szathmari,Carmine Mottolese,Angela Sirigu,Bassem Hiba

doi:10.1016/j.neuroimage.2021.118002

Abstract

The dorso-posterior parietal cortex (DPPC) is a major node of the grasp/manipulation control network. It is assumed to act as an optimal forward estimator that continuously integrates efferent outflows and afferent inflows to modulate the ongoing motor command. In agreement with this view, a recent per-operative study, in humans, identified functional sites within DPPC that: (i) instantly disrupt hand movements when electrically stimulated; (ii) receive short-latency somatosensory afferences from intrinsic hand muscles. Based on these results, it was speculated that DPPC is part of a rapid grasp control loop that receives direct inputs from the hand-territory of the primary somatosensory cortex (S1) and sends direct projections to the hand-territory of the primary motor cortex (M1). However, evidence supporting this hypothesis is weak and partial. To date, projections from DPPC to M1 grasp zone have been identified in monkeys and have been postulated to exist in humans based on clinical and transcranial magnetic studies. This work uses diffusion-MRI tractography in two samples of right- (n = 50) and left-handed (n = 25) subjects randomly selected from the Human Connectome Project. It aims to determine whether direct connections exist between DPPC and the hand control sectors of the primary sensorimotor regions. The parietal region of interest, related to hand control (hereafter designated DPPChand), was defined permissively as the 95% confidence area of the parietal sites that were found to disrupt hand movements in the previously evoked per-operative study. In both hemispheres, irrespective of handedness, we found dense ipsilateral connections between a restricted part of DPPChand and focal sectors within the pre and postcentral gyrus. These sectors, corresponding to the hand territories of M1 and S1, targeted the same parietal zone (spatial overlap > 92%). As a sensitivity control, we searched for potential connections between the angular gyrus (AG) and the pre and postcentral regions. No robust pathways were found. Streamline densities identified using AG as the starting seed represented less than 5 % of the streamline densities identified from DPPChand. Together, these results support the existence of a direct sensory-parietal-motor loop suited for fast manual control and more generally, for any task requiring rapid integration of distal sensorimotor signals.

Highlights

The primate hand is an extraordinarily sophisticated and flexible sensorimotor system
To evaluate the generality of the results obtained from this main sample and to evaluate the existence of potential hemispheric asymmetries related to handedness, we considered an additional population of 25 left-handed subjects
The DPPChand region of interest (ROI) was defined on each individual pial surface, in MNI coordinates, as the 95% confidence area of all the parietal sites that disrupted hand movements when electrically stimulated in our per-operative study (Desmurget et al, 2018)

Summary

Introduction

The primate hand is an extraordinarily sophisticated and flexible sensorimotor system. This skillfulness relies on the contribution of powerful control loops that continuously adjust the ongoing efferent command to compensate for biological (Guigon et al, 2008; Harris and Wolpert, 1998), dynamic (Augurelle et al, 2003; Edin et al, 1992) and contextual (Desmurget and Prablanc, 1997; Paulignan et al, 1991) errors These loops are modeled in the form of a real-time optimal controller that steadily drives neural activity in output motor regions, so as to progressively nullify the distance between the ongoing state of the motor plant, indirectly estimated by integrating sensory inflows and motor outflows (Desmurget and Grafton, 2000; Wolpert et al, 1995) and the goal of the movement (Diedrichsen et al, 2010; Todorov, 2004). During the last decade Transcranial Magnetic Stimulation (TMS) studies have shown, for instance, that transient virtual lesions of the rostral part of the intraparietal sulcus impairs grasping behaviors (Dafotakis et al, 2008; Davare et al, 2007), prevents on-line adjustments of hand shaping (Rice et al, 2007; Rice et al, 2006; Tunik et al, 2005) and bias neural activity in the ventral premotor region (Davare et al, 2010)

Methods

Results

Conclusion