Disentangling Representations of Object and Grasp Properties in the Human Brain

J Neurosci. 2016 Jul 20;36(29):7648-62. doi: 10.1523/JNEUROSCI.0313-16.2016.

Abstract

The properties of objects, such as shape, influence the way we grasp them. To quantify the role of different brain regions during grasping, it is necessary to disentangle the processing of visual dimensions related to object properties from the motor aspects related to the specific hand configuration. We orthogonally varied object properties (shape, size, and elongation) and task (passive viewing, precision grip with two or five digits, or coarse grip with five digits) and used representational similarity analysis of functional magnetic resonance imaging data to infer the representation of object properties and hand configuration in the human brain. We found that object elongation is the most strongly represented object feature during grasping and is coded preferentially in the primary visual cortex as well as the anterior and posterior superior-parieto-occipital cortex. By contrast, primary somatosensory, motor, and ventral premotor cortices coded preferentially the number of digits while ventral-stream and dorsal-stream regions coded a mix of visual and motor dimensions. The representation of object features varied with task modality, as object elongation was less relevant during passive viewing than grasping. To summarize, this study shows that elongation is a particularly relevant property of the object to grasp, which along with the number of digits used, is represented within both ventral-stream and parietal regions, suggesting that communication between the two streams about these specific visual and motor dimensions might be relevant to the execution of efficient grasping actions.

Significance statement: To grasp something, the visual properties of an object guide preshaping of the hand into the appropriate configuration. Different grips can be used, and different objects require different hand configurations. However, in natural actions, grip and object type are often confounded, and the few experiments that have attempted to separate them have produced conflicting results. As such, it is unclear how visual and motor properties are represented across brain regions during grasping. Here we orthogonally manipulated object properties and grip, and revealed the visual dimension (object elongation) and the motor dimension (number of digits) that are more strongly coded in ventral and dorsal streams. These results suggest that both streams play a role in the visuomotor coding essential for grasping.

Keywords: MVPA; fMRI; grasping; motor; representational similarity analysis; visual.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brain / diagnostic imaging
  • Brain / physiology*
  • Brain Mapping
  • Female
  • Hand Strength / physiology*
  • Humans
  • Image Processing, Computer-Assisted
  • Linear Models
  • Magnetic Resonance Imaging
  • Male
  • Oxygen
  • Psychomotor Performance / physiology*
  • Young Adult

Substances

  • Oxygen

Grants and funding