Elsevier

NeuroImage

Volume 36, Issue 2, June 2007, Pages 388-395
NeuroImage

Central control of grasp: Manipulation of objects with complex and simple dynamics

https://doi.org/10.1016/j.neuroimage.2007.01.057Get rights and content

Abstract

We performed whole-brain fMRI to explore the neural mechanisms that contribute to the ability to manipulate an object with complex dynamics. Subjects grasped a weighted flexible ruler and balanced it in an unstable equilibrium position as an archetype of grasping an object with complex dynamics. This was contrasted with squeezing a soft foam ball as an archetype of grasping an object with simple dynamics. We hypothesized that changes in activity in primary motor cortex (MI) would be similar under the two conditions, since muscle activation was matched, which was confirmed. We hypothesized further that the cerebellum would be selectively activated when manipulating the flexible ruler because the ability to make the adjustments necessary to balance the ruler would require an internal dynamics model, represented in the cerebellum. As predicted, the ipsilateral cerebellum was strongly activated when balancing the weighted ruler whereas only moderate activation was found when squeezing the foam ball. We also found evidence for selective activation of areas, previously implicated in tactile object recognition, when holding the flexible ruler. We speculate that these areas, which include secondary somatosensory cortex (SII), Brodmann area 40 and insula, integrate tactile and proprioceptive information in the context of controlling the orientation of the flexible ruler and provide appropriate feedback to MI. We speculate that the failure to find activation of these areas when squeezing the ball was due to the fact that tactile stimulation was entirely self-produced, resulting in the attenuation of cortical sensory activity (Blakemore, S.-J., Wolpert, D.M., Frith, C.D., 1998. Central cancellation of self-produced tickle sensation. Nat. Neurosci. 1, 635–640, Blakemore, S.-J., Frith, C.D., Wolpert, D.M., 2001. The cerebellum is involved in predicting the sensory consequences of action. NeuroReport 12, 1879–1884).

Introduction

The complexity of dynamic interactions between humans and common implements which we employ as tools and instruments can vary widely. Our ability to use implements effectively requires that we be able to hold them despite differences in dynamics. With experience we can quickly change patterns of muscle activation to adjust our grasp for differences in mass, moment of inertia, rigidity or other mechanical properties. This ability is thought to depend on a central representation (internal model) of the dynamics of the interaction between the human subject and the manipulated object (Flanagan and Wing, 1997, Kawato, 1999). By internal dynamics model we mean the neural networks that compute the neural commands to control the movement of the handheld object and compensate for its dynamics.

The cerebellum and primary motor cortex appear to be the regions of the brain most directly implicated in the formation and implementation of internal dynamics models. In particular, the ipsilateral cerebellum shows changes in regional cerebral blood flow during adaptation to novel environmental dynamics that appear to be related to changes in motor error (Nezafat et al., 2001). Other evidence from fMRI studies suggests that the cerebellum is involved in forming and implementing representations of novel transformations between hand and cursor motion (Imamizu et al., 2000, Imamizu et al., 2003), forward models of grip force–load force coupling (Kawato et al., 2003) and dynamics of object manipulation (Milner et al., 2006). Evidence for involvement of primary motor cortex is based primarily on single unit recordings from non-human primates. Studies of changes in manipulation dynamics with non-human primates have reported shifts in the preferred directions of neurons in MI (Li et al., 2001) and to a lesser extent in SMA (Padoa-Schioppa et al., 2004) that develop during adaptation and are retained after washout. However, there are major outputs from the cerebellum to M1 and minor outputs to SMA (Sakai et al., 2002, Kelly and Strick, 2003) so it is possible that underlying changes in cerebellar activity may be responsible for the observed changes in MI and SMA.

To test the hypothesis that cerebellar activity more closely represents implementation of an internal model than does activity in primary motor cortex, we designed an fMRI study which compared brain activity when subjects held an object with simple dynamics and an object with complex dynamics. The former required no internal model to control grasp while the latter required an internal model to adjust the finger forces used in grasping the object for the moment-to-moment control of the object's orientation. From earlier studies, we expected that activity in both primary motor cortex and cerebellum, relative to resting baseline, would increase in proportion to muscle activation (Dettmers et al., 1996, Thickbroom et al., 1998, Ehrsson et al., 2001, Kuhtz-Buschbeck et al., 2001, Dai et al., 2001). However, we predicted that for similar levels of muscle activation we would find little or no difference in primary motor cortex activity, but marked differences in activation of the cerebellum because of its involvement in internal model-based control.

Section snippets

Methods

Seventeen neurologically normal subjects participated in the first experiment. Five of these subjects and five additional subjects participated in the second experiment. Four of these subjects and six additional subjects participated in the third experiment. All subjects gave informed consent to the procedures which were approved by the institutional ethics board and conformed to the Declaration of Helsinki. There were three conditions, corresponding to three tasks performed while lying in the

Results

We report regions where activation in clusters of 5 or more voxels (40 mm3) reached the significance threshold, using the random effects model, corrected for multiple comparisons (p < 0.05). For the complex-simple contrast, we found small regions of significant activation in two regions normally associated with processing of somatosensory activity, namely contralateral somatosensory cortex (SI, area 2) and ipsilateral (right) Brodmann area 40. We found significant activation of the contralateral

Discussion

The complex-simple contrast revealed significant activation only in areas normally associated with processing of somatosensory information. Regions such as SI and thalamus, which were found to have significant activity in the complex-rest contrast, have been previously shown to be activated during control of precision grasp. Somatosensory association areas such as SII, Brodmann area 40 and insula, which were found to have significant activation in the complex-rest or complex-simple contrast,

Acknowledgments

This work was supported by NICT and NSERC. We thank S. Masuda for assisting in the second experiment.

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