Elsevier

Human Movement Science

Volume 26, Issue 4, August 2007, Pages 590-616
Human Movement Science

Evidence for a distributed hierarchy of action representation in the brain

https://doi.org/10.1016/j.humov.2007.05.009Get rights and content

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.

Section snippets

Introduction: Action hierarchy

A fundamental problem in motor neuroscience is to understand how the nervous system selects and organizes motor elements that, when combined, result in the completion of a temporally distant goal. Achieving this level of behavioral complexity across a broad range of contingencies, irrespective of whether a tool is used, sets humans apart from other animals. This is a key cognitive mechanism that is arguably equivalent to language in importance. How the brain accomplishes action organization

Historic perspective

The modern era for understanding the organization of complex motor behavior can be traced back in part to Nicholai Bernstein (Bernstein, 1996). He was one of the first to recognize a need for integrating evolutionary biology, musculoskeletal form and function, biomechanics and observations of goal driven behavior to explain motor behavior. He emphasized the notion of a control hierarchy spanning multiple levels of the neuroaxis, based on increasing complexity from muscle to spine to brain, with

Prehension

Studies of normal prehension have played an essential role in demonstrating modularity in the organization of reach and grasp as separable, but interacting processes. In addition, prehension remains an important experimental paradigm for demonstrating how behavior is shaped in anticipation of future motor outcomes. During a reach and grasp, the arm, hand and digits move toward the desired object in a highly structured behavioral pattern, with kinematic features reflecting the object’s size,

Computational models

Given the many observations that actions are organized with respect to distal goals, what is the cognitive or computational framework within which this is achieved? Although the answer to this remains unknown, there are a number of important approaches to consider. A motor program could be played out like a computer algorithm or tape recording. Putative algorithms include feedforward control for sequences of movements such as typing or writing (Keele et al., 1995), action schema, and

Ideomotor apraxia

Neural evidence that there are distinct brain structures for organizing movement in terms of relative hierarchy, including action goals, began with studies of apraxic patients. In building a case for what constituted apraxia versus other clinical syndromes a century ago, Liepmann (1988) argued that distinctions should be made at both a behavior level and in the concomitant localization of lesions in the brain. From the original meaning of Πραττειν, literally to act, that is, to move

The mirror neuron system

There is now strong evidence that observing an action by another, such as grasping an object, using a tool, or performing a whole body movement such as dance recruits a widely distributed network of inferior prefrontal, premotor, parietal and superior temporal cortex (Chao and Martin, 2000, Cross et al., 2006, Grafton et al., 1996, Grafton et al., 1997). Broadly speaking, these areas that are responsive during action observation can be referred to as an action resonance network. Subsets of

Repetition suppression

We recently employed a method to distinguish levels of action representation based on a phenomenon called repetition suppression (RS). RS has been extensively used in studies of visual representations (Grill-Spector and Malach, 2001, Kourtzi and Kanwisher, 2000), where it is sometimes referred to as fMRI-adaptation. Repetition suppression is based on reduced physiologic responses to repeated stimuli. Fig. 2 is an example of an RS paradigm from one of our fMRI studies. The phenomenon is not

Acknowledgement

Supported by PHS grants NS 33504, NS 44393 and the James S. McDonnell Foundation.

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