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The Journal of Neuroscience, February 7, 2007, 27(6):1346-1355; doi:10.1523/JNEUROSCI.3822-06.2007

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Behavioral/Systems/Cognitive
A Reevaluation of the Inverse Dynamic Model for Eye Movements

Andrea M. Green,¹ Hui Meng,² and Dora E. Angelaki²

¹Département de Physiologie, Université de Montréal, Montréal, Québec, Canada H3T 1J4, and ²Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110

Correspondence should be addressed to Dr. Andrea Green, Département de Physiologie, Université de Montréal, 2960 Chemin de la Tour, Room 2140, Montréal, Québec, Canada H3T 1J4. Email: andrea.green{at}umontreal.ca

To construct an appropriate motor command from signals that provide a representation of desired action, the nervous system must take into account the dynamic characteristics of the motor plant to be controlled. In the oculomotor system, signals specifying desired eye velocity are thought to be transformed into motor commands by an inverse dynamic model of the eye plant that is shared for all types of eye movements and implemented by a weighted combination of eye velocity and position signals. Neurons in the prepositus hypoglossi and adjacent medial vestibular nuclei (PH-BT neurons) were traditionally thought to encode the "eye position" component of this inverse model. However, not only are PH-BT responses inconsistent with this theoretical role, but compensatory eye movement responses to translation do not show evidence for processing by a common inverse dynamic model. Prompted by these discrepancies between theoretical notions and experimental observations, we reevaluated these concepts using multiple-frequency rotational and translational head movements. Compatible with the notion of a common inverse model, we show that PH-BT responses are unique among all premotor cell types in bearing a consistent relationship to the motor output during eye movements driven by different sensory stimuli. However, because their responses are dynamically identical to those of motoneurons, PH-BT neurons do not simply represent an internal component of the inverse model, but rather its output. They encode and distribute an estimate of the motor command, a signal critical for accurate motor execution and learning.

Key words: internal model; eye movement; vestibular; efference copy; sensorimotor; motor control

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Received Sept. 1, 2006; revised Nov. 27, 2006; accepted Dec. 20, 2006.

Correspondence should be addressed to Dr. Andrea Green, Département de Physiologie, Université de Montréal, 2960 Chemin de la Tour, Room 2140, Montréal, Québec, Canada H3T 1J4. Email: andrea.green{at}umontreal.ca

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