Two action systems in the human brain

Abstract

The distinction between dorsal and ventral visual processing streams, first proposed by Ungerleider and Mishkin (1982) and later refined by Milner and Goodale (1995) has been elaborated substantially in recent years, spurred by two developments. The first was proposed in large part by Rizzolatti and Matelli (2003) and is a more detailed description of the multiple neural circuits connecting the frontal, temporal, and parietal cortices. Secondly, there are a number of behavioral observations that the classic "two visual systems" hypothesis is unable to accommodate without additional assumptions. The notion that the Dorsal stream is specialized for "where" or "how" actions and the Ventral stream for "What" knowledge cannot account for two prominent disorders of action, limb apraxia and optic ataxia, that represent a double dissociation in terms of the types of actions that are preserved and impaired. A growing body of evidence, instead, suggests that there are at least two distinct Dorsal routes in the human brain, referred to as the "Grasp" and "Use" systems. Both of these may be differentiated from the Ventral route in terms of neuroanatomic localization, representational specificity, and time course of information processing.

Keywords: Ventral stream; Ventro-dorsal and dorso-dorsal stream; “Use” and “Grasp” systems.

Fig. 1

Dorso-dorsal stream (A) and ventro-dorsal stream (B) in macaque (adopted from Rizzolatti et al. (1998) and Rizzolatti and Matelli (2003)).

Fig. 2

Diffusion Tensor Imaging (DTI) analysis of connections between the area aIPS and the area cIPS, the ventral premotor conrtex and the infero-temporal cortex (adopted from Pisella et al. (2006) and Binkofski et al. (2007))

Fig. 3

Shematic relative location of the dorso-dorsal (red) and the ventro-dorsal (green) sub-streams of the dorsal stream, as well as the ventral stream (blue) (from Binkofski and Fink (2005)).

Fig. 4

Initiation times to grasp or indicate hand posture for using common objects as a function of object type and task order. Grasping (left) is slower for conflict objects when preceded by the ‘use’ task than when not, indicating long lasting use representations. Use (right) is slower for conflict objects regardless of task order, indicating obligatory activation of grasp representations that is short-lasting (adapted from Jax and Buxbaum (2010)).

Fig. 5

Time course of gaze fixations on competitor objects (dashed line) and unrelated objects (dotted line) when locating target objects (solid line) in “Saw” and “Picked up” verbal contexts. In the ‘picked up’ context (right), competitor activation is shifted earlier, suggesting facilitation of processing of competitor objects that are picked up similarly to the targets. Adapted from Lee et al. (2012).