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The Journal of Neuroscience, March 12, 2008, 28(11):2804-2813; doi:10.1523/JNEUROSCI.5300-07.2008

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Behavioral/Systems/Cognitive
Adaptive Control of Saccades via Internal Feedback

Haiyin Chen-Harris,¹ Wilsaan M. Joiner,¹ Vincent Ethier,¹ David S. Zee,² and Reza Shadmehr¹

Departments of ¹Biomedical Engineering and ²Neurology, Johns Hopkins School of Medicine, Baltimore, Maryland 21205

Correspondence should be addressed to Reza Shadmehr, Johns Hopkins School of Medicine, 410 Traylor Building, 720 Rutland Avenue, Baltimore, MD 21205. Email: reza{at}bme.jhu.edu

Ballistic movements like saccades require the brain to generate motor commands without the benefit of sensory feedback. Despite this, saccades are remarkably accurate. Theory suggests that this accuracy arises because the brain relies on an internal forward model that monitors the motor commands, predicts their sensory consequences, and corrects eye trajectory midflight. If control of saccades relies on a forward model, then the forward model should adapt whenever its predictions fail to match sensory feedback at the end of the movement. Using optimal feedback control theory, we predicted how this adaptation should alter saccade trajectories. We trained subjects on a paradigm in which the horizontal target jumped vertically during the saccade. With training, the final position of the saccade moved toward the second target. However, saccades became increasingly curved, i.e., suboptimal, as oculomotor commands were corrected on-line to steer the eye toward the second target. The adaptive response had two components: (1) the motor commands that initiated the saccades changed slowly, aiming the saccade closer to the jumped target. The adaptation of these earliest motor commands displayed little forgetting during the rest periods. (2) Late in saccade trajectory, another adaptive response steered it still closer to the jumped target, producing curvature. Adaptation of these late motor commands showed near-complete forgetting during the rest periods. The two components adapted at different timescales, with the late-acting component displaying much faster rates. It appears that in controlling saccades, the brain relies on an internal feedback that has the characteristics of a fast-adapting forward model.

Key words: saccade adaptation; forward model; internal feedback; optimal control; curved saccades; fatigue

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Received July 20, 2007; revised Jan. 9, 2008; accepted Jan. 28, 2008.

Correspondence should be addressed to Reza Shadmehr, Johns Hopkins School of Medicine, 410 Traylor Building, 720 Rutland Avenue, Baltimore, MD 21205. Email: reza{at}bme.jhu.edu

Related articles in J. Neurosci.:

Optimally Straight and Optimally Curved Saccades

Mark R. Harwood and James P. Herman
J. Neurosci. 2008 28: 7455-7457. [Full Text]  

This article has been cited by other articles:

				M. R. Harwood and J. P. Herman Optimally Straight and Optimally Curved Saccades J. Neurosci., July 23, 2008; 28(30): 7455 - 7457. [Full Text] [PDF]

				V. Ethier, D. S. Zee, and R. Shadmehr Spontaneous Recovery of Motor Memory During Saccade Adaptation J Neurophysiol, May 1, 2008; 99(5): 2577 - 2583. [Abstract] [Full Text] [PDF]

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