Optimal Sensorimotor Control in Eye Movement Sequences

Abstract

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 Ͻ30% 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.

Optimal and Suboptimal Use of Postsaccadic Vision in Sequences of Saccades

“…It is thus possible that a common mechanism of cue combinations underlies both perceptual and sensorimotor functions. The value of the maximum weight (obtained in Targetϩ Background) is consistent with the conclusions of van Beers (2007) and Munuera et al (2009): even in a structured visual environment, visual noise dominates motor execution noise. However, this weight was smaller than expected (14% in condition Target vs predicted ϳ40%) from the noise estimates of van Beers (2007), if vision is the only sensory modality contributing to the postsaccadic update.…”

“…where m 2 is the variance of the motor execution noise, and v 2 is the variance of the localization of the visual scene before S1 (Munuera et al, 2009). If there is no motor noise, ϭ 0.…”

“…When available, visual information is a complementary source of information. Presaccadic and postsaccadic information can be optimally combined to determine target position (Vaziri et al, 2006); their comparison can also be used in combination with the efference copy to update the internal estimate of the state of the oculomotor system (Munuera et al, 2009). This latter study showed that the weight of visual target information is consistent with an optimal integration of sensory information with respect to its noise (visual noise) compared with the noise in the efference copy (motor noise).…”

“…However, the 2009 study (Munuera et al, 2009) was subject to some methodological limitations. In particular, stereotyped visual stimuli could have biased the subjects toward cognitive strategies.…”

Human thalamus contributes to perceptual stability across eye movements

“…Targeting errors from noise originating in processing steps upstream the level at which a putative corollary discharge signal is fed back should therefore be taken into account. The perceptual report should then be largely independent from the associated oculomotor targeting error (24,25).…”