Neural systems that control movement maintain accuracy by adaptively altering motor commands in response to errors. It is often assumed that the error signal that drives adaptation is equivalent to the sensory error observed at the conclusion of a movement; for saccades, this is typically the visual (retinal) error. However, we instead propose that the adaptation error signal is derived as the difference between the observed visual error and a realistic prediction of movement outcome. Using a modified saccade-adaptation task in human subjects, we precisely controlled the amount of error experienced at the conclusion of a movement by back-stepping the target so that the saccade is hypometric (positive retinal error), but less hypometric than if the target had not moved (smaller retinal error than expected). This separates prediction error from both visual errors and motor corrections. Despite positive visual errors and forward-directed motor corrections, we found an adaptive decrease in saccade amplitudes, a finding that is well-explained by the employment of a prediction-based error signal. Furthermore, adaptive changes in movement size were linearly correlated to the disparity between the predicted and observed movement outcomes, in agreement with the forward-model hypothesis of motor learning, which states that adaptation error signals incorporate predictions of motor outcomes computed using a copy of the motor command (efference copy).
Shelhamer, Mark and Wilsaan M. Joiner. Saccades exhibit abrupt transition between reactive and predictive, predictive saccade sequences have long-term correlations. J Neurophysiol 90: 2763-2769, 2003; 10.1152/jn.00478.2003. To compensate for neural delays, organisms require predictive motor control. We investigated the transition between reaction and prediction in saccades (rapid eye movements) to periodically paced targets. Tracking at low frequencies (0.2-0.3 Hz) is reactive (eyes lag target) and at high frequencies (0.9 -1.0 Hz) is predictive (eyes anticipate target); there is an abrupt rather than smooth transition between the two modes (a "phase transition," as found in bistable physical systems). These behaviors represent stable modes of the oculomotor control system, with attendant rapid switching between the neural pathways underlying the different modes. Furthermore, predictive saccades exhibit long-term correlations (slow decay of the autocorrelation function, manifest as a 1/f ␣ spectrum). This indicates that predictive trials are not independent. The findings have implications for the understanding of predictive motor control: predictive performance during a given trial is influenced by a feedback process that takes into account the latency of previous trials.
Studies on motor learning typically present a constant adaptation stimulus, corresponding to the desired final adaptive state. Studies of the auditory and optokinetic systems provide compelling evidence that neural plasticity is enhanced when the error signal driving adaptation is instead adjusted gradually throughout training. We sought to determine whether the angular vestibulo-ocular reflex (aVOR) may be adaptively increased using an incremental velocity error signal (IVE) compared with a conventional constant and large velocity-gain demand (x2). We compared the magnitude of aVOR gain change for these two paradigms across different motion contexts (active and passive). Seven individuals with normal vestibular function and six individuals with unilateral vestibular hypofunction (UVH) were exposed to the IVE and x2 (“control”) aVOR demand tasks. Each subject participated in 10 epochs of 30 active head impulses over a 15 min aVOR gain increase training session separately for the IVE and x2 paradigms, separated by either seven days (normal subjects) or 14 days (UVH subjects). For both normal and UVH subjects, both paradigms led to aVOR gain increase during the training session. For the normal subjects, the IVE paradigm led to larger aVOR gain change after training compared to the x2 paradigm, for both active (mean 17.3 ± 4% vs. mean 7.1 ± 9%, P = 0.029) and passive (mean 14.2 ± 5% vs. 4.5 ± 8%, P = 0.018) head impulses. For subjects with UVH, IVE produced a greater change in aVOR gain for active head impulses (mean 18.2 ± 9.2% vs. mean –6 ± 3.8%, P = 0.003). However, aVOR gains for passive head impulses were less consistent after IVE, with only two subjects displaying greater aVOR gain with this incremental paradigm. Some individuals generated compensatory saccades that occurred in the same direction of the deficient aVOR during either training paradigm. Our data suggest that the aVOR is modifiable when the velocity error signal is presented incrementally, and that this adaptation stimulus is particularly effective in the case of unilateral vestibular hypofunction. This has implications for programs of vestibular rehabilitation, where active head rotation is prescribed as a means to improve gaze stability.
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