Similar brain networks for detecting visuo-motor and visuo-proprioceptive synchrony

Abstract

The ability to recognize feedback from own movement as opposed to the movement of someone else is important for motor control and social interaction. The neural processes involved in feedback recognition are incompletely understood. Two competing hypotheses have been proposed: the stimulus is compared with either (a) the proprioceptive feedback or with (b) the motor command and if they match, then the external stimulus is identified as feedback. Hypothesis (a) predicts that the neural mechanisms or brain areas involved in distinguishing self from other during passive and active movement are similar, whereas hypothesis (b) predicts that they are different. In this fMRI study, healthy subjects saw visual cursor movement that was either synchronous or asynchronous with their active or passive finger movements. The aim was to identify the brain areas where the neural activity depended on whether the visual stimulus was feedback from own movement and to contrast the functional activation maps for active and passive movement. We found activity increases in the right temporoparietal cortex in the condition with asynchronous relative to synchronous visual feedback from both active and passive movements. However, no statistically significant difference was found between these sets of activated areas when the active and passive movement conditions were compared. With a posterior probability of 0.95, no brain voxel had a contrast effect above 0.11% of the whole-brain mean signal. These results do not support the hypothesis that recognition of visual feedback during active and passive movement relies on different brain areas.

Introduction

Although in everyday life people rarely are in doubt whether a visual object is an image of their moving hand or not, there are conditions where the visual feedback is more difficult to identify—for instance when two surgeons operate together and watch their hand movements in a video display from various directions.

Defective feedback recognition has been found to occur more frequently in patients with apraxia (Sirigu et al., 1999) or schizophrenia (Daprati et al., 1997, Johns et al., 2001) than in control groups, suggesting that correct detection of movement ownership may be important for skilled movement and social interaction.

Despite the interest in the topic, the neural processes involved in feedback recognition are incompletely understood. Two competing hypotheses have been proposed. The stimulus is compared with either (a) the proprioceptive feedback (Guillaume, 1971) or with (b) the motor command (Frith, 1996) and if they match, then the external stimulus is identified as feedback.

Hypothesis (b) has been detailed in the framework of the brain's forward model. The forward model is a system that estimates the sensory consequences of a motor command (Wolpert et al., 1995), allowing sensory events that match this estimate to be cancelled out (Blakemore et al., 1999, Shergill et al., 2003). Thus, hypothesis (b) predicts differences in brain activity when movements are accompanied by congruent versus incongruent sensory feedback. It also predicts that this difference would appear only during conditions with active movements, when the motor command allows to estimate a sensory outcome and not during conditions with passive movements, when the sensory feedback cannot be anticipated. On the contrary, hypothesis (a) predicts that the brain areas involved in distinguishing self from other during passive and active movement are similar, because proprioception would be available in both conditions.

Several neuroimaging studies have identified brain areas that are sensitive to the congruency of visual feedback from active (Blakemore et al., 1998, Farrer and Frith, 2002, Leube et al., 2003) or passive (Balslev et al., 2005, Shimada et al., 2005) movements. The differences in the functional brain maps highlighted by these studies may reflect a genuine difference in the brain mechanisms engaged by the detection of feedback during the processing of active and passive movement, or may merely have been caused by differences in the experimental paradigms. The relative lack of overlap between the findings within the same category of studies (e.g. studies that have used active movements) strongly suggest that the functional activity maps depend on the particularities of the task. The aim of this fMRI study was to present a similar task in both the active and passive movement condition, so that the functional brain maps for detection of visuo-motor and visuo-proprioceptive synchrony could be directly compared.