Elsevier

NeuroImage

Volume 31, Issue 1, 15 May 2006, Pages 264-278
NeuroImage

Information processing in human parieto-frontal circuits during goal-directed bimanual movements

https://doi.org/10.1016/j.neuroimage.2005.11.033Get rights and content

Abstract

It is known that, in macaques, movements guided by somatosensory information engage anterior parietal and posterior precentral regions. Movements performed with both visual and somatosensory feedback additionally activate posterior parietal and anterior precentral areas. It remains unclear whether the human parieto-frontal circuits exhibit a similar functional organization.

Here, we employed a directional interference task requiring a continuous update of sensory information for the on-line control of movement direction, while brain activity was measured by functional magnetic resonance imaging (fMRI). Directional interference arises when bimanual movements occur along different directions in joint space. Under these circumstances, the presence of visual information does not substantially alter performance, such that we could vary the amount and type of sensory information used during on-line guidance of goal-directed movements without affecting motor output.

Our results confirmed that in humans, as in macaques, movements guided by somatosensory information engages anterior parietal and posterior precentral regions, while movements performed with both visual and somatosensory information activate posterior parietal and anterior precentral areas. We provide novel evidence on how the interaction of specific portions of the dorsal parietal and precentral cortex in the right hemisphere might generate spatial representations by integrating different sensory modalities during goal-directed movements.

Introduction

Single unit and lesion studies in the macaque have revealed how parieto-precentral circuits can generate spatial representations from sensory information during goal-directed actions (Rizzolatti et al., 1998, Johnson et al., 1996, Wise et al., 1997, Rushworth et al., 1997). Furthermore, it has been shown that different sensory modalities are processed within distinct parieto-frontal circuits (Rizzolatti et al., 1998, Johnson et al., 1996, Burnod et al., 1999) (Fig. 3A). More specifically, anterior parietal areas PE and PEip respond to somatosensory stimuli (Iwamura and Tanaka, 1996, Lacquaniti et al., 1995, Johnson et al., 1996) and project to posterior precentral cortex [medio-caudal portion of area F2] (Johnson et al., 1996, Rizzolatti et al., 1998, Fogassi et al., 1999, Lacquaniti et al., 1995, Marconi et al., 2001). Posterior parietal areas MIP, PEc, and V6A respond additionally to visual stimuli (Battaglia-Mayer et al., 2001, Galletti et al., 2001, Johnson et al., 1996, Colby and Duhamel, 1991, Galletti et al., 2003, Breveglieri et al., 2002) and project to anterior precentral cortex [rostro-lateral portion of F2] (Matelli et al., 1998, Rizzolatti et al., 1998, Marconi et al., 2001, Johnson et al., 1996, Fogassi et al., 1999). Despite growing evidence supporting a close functional correspondence in the organization of parietal and frontal cortex of macaques and humans (Bremmer et al., 2001, Passingham, 1998, Sereno et al., 2001, Toni et al., 2001b), to date, there has been no empirical support for a similar modality-specific segregation of the human parieto-frontal circuitry in the context of goal-directed movements. A few imaging studies have explored this issue by using simple pointing paradigms (Ellermann et al., 1998, Inoue et al., 1998, Lacquaniti et al., 1997, Connolly et al., 2000), but provided no evidence for spatially independent sensorimotor processing streams in the parieto-frontal system. However, the scope of these negative results might be limited to the experimental setting of these studies, since the semi-ballistic nature of simple pointing paradigms appears inadequate for evoking on-line sensory guidance of movement in space.

Here, we aim at understanding the specific contributions of superior parietal and dorsal precentral cortex to sensorimotor processing. Building on the known functional organization of parieto-frontal circuits in macaques, we have tested the hypothesis that in humans, as in macaques, performance of movements guided by somatosensory information engages anterior parietal and posterior precentral regions. Conversely, movements performed with both visual and somatosensory information should additionally activate posterior parietal and anterior precentral areas. To ensure that sensory information was actually used for on-line guidance of movements, rather than for planning semi-ballistic movements, we have exploited the behavioral phenomenon of directional interference. Directional interference emerges when two limbs are moved simultaneously along directionally incompatible trajectories, as when one tries to concurrently draw a vertical line with the left arm and a horizontal line with the right arm. Under these circumstances, a mutual bias of movement directions automatically emerges between the limbs movements (Swinnen et al., 2001). Consequently, moving along incompatible directions requires subjects to permanently monitor the limbs' positions in space to prevent limb trajectories from becoming substantially biased. Here, we induced directional interference by using combinations of cyclical, metronome-paced ‘line-drawing’ movements (i.e., moving along a vertical line at all times) and ‘star-drawing’ movements (i.e., moving along systematically varying orientations deviating either +45, 90 or −45° from the vertical—see Fig. 1). We applied functional magnetic resonance imaging (fMRI) while subjects performed either the directionally compatible StarStar task (i.e., symmetrical star-drawing with the left and the right hand) or the directionally incompatible LineStar/StarLine tasks (i.e., line-drawing with one hand while star-drawing with the other hand). These tasks were performed either under somatosensory guidance only or with additional visual information. Continuous kinematic measurements obtained during task performance in the scanner confirmed that the presence of visual information does not substantially alter the behavioral effects of directional interference (Puttemans et al., 2004). This singular feature of directional interference tasks makes it possible to vary the amount and type of sensory information used during movement performance without affecting motor output. Therefore, we have exploited directional interference to drive subjects to rely on sensory guidance of movements, while manipulating the type of sensory information available for on-line control of motor performance. By combining this robust psychophysical protocol with fMRI, we have been able to isolate modality-specific brain responses during on-line guidance of goal-directed movements, other factors being equal.

Section snippets

Subjects

Eleven volunteers (6 females, 5 males, aged 22 ± 2 (S.D.) years) participated in the experiment. All were right-handed (Oldfield, 1971), naïve with respect to the task and had normal vision. None of them participated in regular musical training. All subjects gave written informed consent before participating in the experiment which was approved by the local ethical committee of K.U.Leuven. Subjects were paid for their services.

Experimental setup

Subjects lay supine in the scanner with their upper arms next to the

Behavioral data

Directional interference was quantified by mean orientation error (αError) and orientation variability (αSD), averaged between wrists. Both αError and αSD were significantly increased during the execution of the directionally incompatible (StarLine/LineStar) as compared to the directionally compatible tasks (StarStar) (F1,10 > 9.3, P < 0.05; Figs. 2A, B). During the incompatible tasks, interference was particularly high when subjects had to trace non-parallel orientations, reaching the highest

Discussion

We have manipulated the availability of visual information during performance of a bimanual directional interference task in order to assess the spatial segregation of modality-specific neural activity in the human parieto-frontal circuitry. The behavioral results confirm that the inter-limb bias in the execution of different movement directions (directional interference) is indifferent to the presence of visual information. However, the imaging results indicate that visual information strongly

Conclusions

We have characterized the spatial distribution and inter-regional couplings of modality-specific responses in the human superior parietal and dorsal precentral cortex during the integration of sensory information to guide goal-directed movements. We confirmed that in humans, as in macaques, performance of movements guided by somatosensory information engages anterior parietal and posterior precentral regions, while movements performed with both visual and somatosensory feedback activate

Acknowledgments

This study was supported by the Flanders Fund for Scientific Research (FWO Project- G.0460.04) and the Research Fund K.U.Leuven (OT/03/61).

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