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The Journal of Neuroscience, March 11, 2009, 29(10):3026-3035; doi:10.1523/JNEUROSCI.1169-08.2009

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Behavioral/Systems/Cognitive
Optimal Sensorimotor Control in Eye Movement Sequences

Jérôme Munuera,1 Pierre Morel,1,2,3 Jean-René Duhamel,1 and Sophie Deneve2,3

1Centre de Neuroscience Cognitive, CNRS–Université de Lyon (UMR5229), 69675 Bron, France, 2Group for Neural Theory, Département d'Etudes Cognitives, Ecole Normale Supérieure, 75005 Paris, France, and 3Groupe Neuroscience, équipe accueil, Collège de France, 75005 Paris, France

Correspondence should be addressed to Sophie Deneve, Group for Neural Theory (GNT), 3, rue d'Ulm, 75005 Paris, France. Email: sophie.deneve{at}ens.fr

Fast and accurate motor behavior requires combining noisy and delayed sensory information with knowledge of self-generated body motion; much evidence indicates that humans do this in a near-optimal manner during arm movements. However, it is unclear whether this principle applies to eye movements. We measured the relative contributions of visual sensory feedback and the motor efference copy (and/or proprioceptive feedback) when humans perform two saccades in rapid succession, the first saccade to a visual target and the second to a memorized target. Unbeknownst to the subject, we introduced an artificial motor error by randomly "jumping" the visual target during the first saccade. The correction of the memory-guided saccade allowed us to measure the relative contributions of visual feedback and efferent copy (and/or proprioceptive feedback) to motor-plan updating. In a control experiment, we extinguished the target during the saccade rather than changing its location to measure the relative contribution of motor noise and target localization error to saccade variability without any visual feedback. The motor noise contribution increased with saccade amplitude, but remained <30% of the total variability. Subjects adjusted the gain of their visual feedback for different saccade amplitudes as a function of its reliability. Even during trials where subjects performed a corrective saccade to compensate for the target-jump, the correction by the visual feedback, while stronger, remained far below 100%. In all conditions, an optimal controller predicted the visual feedback gain well, suggesting that humans combine optimally their efferent copy and sensory feedback when performing eye movements.

Received March 18, 2008; revised Dec. 12, 2008; accepted Dec. 22, 2008.

Correspondence should be addressed to Sophie Deneve, Group for Neural Theory (GNT), 3, rue d'Ulm, 75005 Paris, France. Email: sophie.deneve{at}ens.fr






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