Evidence for a distributed hierarchy of action representation in the brain
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.
References (153)
- et al.
Synthetic brain imaging: Grasping, mirror neurons and imitation
Neural Networks
(2000) - et al.
fMRI investigation of cortical and subcortical networks in the learning of abstract and effector-specific representations of motor sequences
NeuroImage
(2006) - et al.
The mirror neuron system and action recognition
Brain and Language
(2004) - et al.
Neural circuits underlying imitation learning of hand actions: An event-related fMRI study
Neuron
(2004) - et al.
Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI
Neuron
(1998) - et al.
Representation of manipulable man-made objects in the dorsal stream
NeuroImage
(2000) - et al.
Building a motor simulation de novo: Observation of dance by dancers
NeuroImage
(2006) - et al.
Forward modeling allows feedback control for fast reaching movements
Trends in Cognitive Science
(2000) - et al.
Prediction precedes control in motor learning
Current Biology
(2003) - et al.
Prehension movements in a patient (AC) with posterior parietal cortex damage and posterior callosal section
Brain and Cognition
(2006)