Evidence for a distributed hierarchy of action representation in the brain

Abstract

Complex human behavior is organized around temporally distal outcomes. Behavioral studies based on tasks such as normal prehension, multi-step object use and imitation establish the existence of relative hierarchies of motor control. The retrieval errors in apraxia also support the notion of a hierarchical model for representing action in the brain. In this review, three functional brain imaging studies of action observation using the method of repetition suppression are used to identify a putative neural architecture that supports action understanding at the level of kinematics, object centered goals and ultimately, motor outcomes. These results, based on observation, may match a similar functional-anatomic hierarchy for action planning and execution. If this is true, then the findings support a functional-anatomic model that is distributed across a set of interconnected brain areas that are differentially recruited for different aspects of goal-oriented behavior, rather than a homogeneous mirror neuron system for organizing and understanding all behavior.

Fig. 1

The visuomotor brain. All cortical areas showing increased activity during compensatory visuomotor tracking with the right hand relative to rest are shown in color, superimposed on a population based surface atlas of the human brain (PALS dataset and Caret visualization tools (http://brainmap.wustl.edu/caret). Data are from 8 participants, left column is right hemisphere, right column is left hemisphere, upper row is medial surface (inverted).

Fig. 2

Example of trial ordering in a series of repetition suppression experiments. In a given sequence, when a stimulus of a given class, such as an object is repeated (Row B), there is reduction of BOLD related responses (Row A). Similar effects apply for different types of objects (Row C). The prediction is that different areas will show RS effects for outcomes of actions (Row D, E) and these can be separated from lower level features such as grip, trajectory and means.

Fig. 3

Anatomic substrates of action observation hierarchy. Repetition effects for low-level kinematics, such as hand trajectory, grip size and object movement are localized to visual association cortex including inferior occipital cortex and the posterior superior parietal cortex (parietal reach region). RS for object-centered goals strongly modulates the anterior intraparietal sulcus and left ventral premotor cortex. Sensitivity to the outcome of an action overlaps to a certain degree with goal-object areas, but also strongly modulates activity in bilateral inferior parietal lobule and right ventral premotor cortex. Data are adapted from three separate RS experiments (Hamilton & Grafton, 2006; Hamilton & Grafton, in press; Hamilton & Grafton 2007).