Abstract

Reaching to a location in space is supported by a cortical network that operates in a variety of reference frames. Computational models and recent fMRI evidence suggest that this diversity originates from neuronal populations dynamically shifting between reference frames as a function of task demands and sensory modality. In this human fMRI study, we extend this framework to nonmanipulative grasping movements, an action that depends on multiple properties of a target, not only its spatial location. By presenting targets visually or somaesthetically, and by manipulating gaze direction, we investigate how information about a target is encoded in gaze- and body-centered reference frames in dorsomedial and dorsolateral grasping-related circuits. Data were analyzed using a novel multivariate approach that combines classification and cross-classification measures to explicitly aggregate evidence in favor of and against the presence of gaze- and body-centered reference frames. We used this approach to determine whether reference frames are differentially recruited depending on the availability of sensory information, and where in the cortical networks there is common coding across modalities. Only in the left anterior intraparietal sulcus (aIPS) was coding of the grasping target modality dependent: predominantly gaze-centered for visual targets and body-centered for somaesthetic targets. Left superior parieto-occipital cortex consistently coded targets for grasping in a gaze-centered reference frame. Left anterior precuneus and premotor areas operated in a modality-independent, body-centered frame. These findings reveal how dorsolateral grasping area aIPS could play a role in the transition between modality-independent gaze-centered spatial maps and body-centered motor areas.

Highlights

  • Parietofrontal neurons involved in reaching to a location in space operate in a variety of reference frames (Battaglia-Mayer et al, 2003; McGuire and Sabes, 2011; Buchholz et al, 2013)

  • Regions of interest Because we had clear hypotheses on the cortical pathways involved in planning right-handed grasping movements, we focused our analyses on five regions of interest (ROIs) in the left hemisphere

  • We investigated the reference frames in which parietal and frontal regions operate during the planning of grasping movements toward visual and somaesthetic targets

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Summary

Introduction

Parietofrontal neurons involved in reaching to a location in space operate in a variety of reference frames (Battaglia-Mayer et al, 2003; McGuire and Sabes, 2011; Buchholz et al, 2013). Theoretical modeling and behavioral evidence has suggested that these reference frames can be dynamically weighted according to task demands and sensory input (Pouget and Snyder, 2000; Beurze et al, 2007; McGuire and Sabes, 2009). Recent neurophysiological work (Bernier and Grafton, 2010) has shown how sensory input influences the contributions of different parietofrontal regions while subjects reached out, by rotating their wrist, to touch visual or proprioceptive targets with their right index finger. By changing the fixation point relative to the target, that study showed that the anterior precuneus encoded the motor goal for visual targets selectively in gaze-centered (GC) coordinates, while other parietofrontal areas showed a mixture of GC and body-centered (BC) encoding. Reaching to proprioceptive targets revealed negligible gaze-centered encoding but considerable bodycentered encoding throughout the parietofrontal network. Here we investigate how task demands affect these modality-dependent reference frames within the grasping network

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