Humans have a remarkable ability to make predictive movements in order to overcome delays in neural processing, and to adapt to changes due to aging and disease. In each case, proper functioning relies on the detection and processing of sensory error information in order to properly program future behavior. We propose a new approach to presenting error feedback, to improve prediction and adaptation. When presented with periodically paced visual targets paced at about 1 Hz, normal subjects naturally make predictive saccades - they are triggered before visual feedback from a given target, with latencies of -100 to +100 msec. Sequences of predictive saccades are correlated: performance of past saccades is stored and taken into account in the timing of subsequent saccades. Initial evidence in patients with cerebellar deficits is that they have deficiencies in making these predictive movements, and that this is due at least in part to deficiencies in monitoring, storing, and processing the errors of previous movements. The ultimate goal of this research program is to present saccade error information to these patients in new ways, to help them improve predictive-saccade timing and accuracy. Our approach is to augment the normal visual error from each saccade with auditory information or with visual information in a different form, and further to present error information that has been accumulated over several previous trials rather than just the most recent. The research plan has four aims. First, determine the effectiveness of augmented feedback for control of predictive-saccade timing. We will supply augmented auditory feedback of timing error to the subject on each trial, to drive timing error to a desired value and to decrease its variability. This feedback is in the form of a beep generated when a saccade is generated or when its timing falls within a desired range. Second, increase correlations between consecutive predictive saccades. These correlations occur naturally in normal subjects, and reflect the fact that previous performance is used to program subsequent movements. We will determine if there is a performance advantage to these correlations, and attempt to increase their extent by providing error feedback based on timing error accumulated over several previous saccades rather than the single preceding one. Third, use similar methods to control endpoints (amplitudes) of predictive saccades, using error feedback of position errors. Fourth, use similar methods to improve the ability to adapt to a double-step stimulus: a visual target moves as the eyes approach it, and after a period of adaptation the eyes make a saccade to the displaced target position when presented with a target at the initial location. By providing augmented feedback based on displaced target position, we hope to improve the rate and extent of this adaptation. All procedures will be performed on normals and cerebellar patients with deficits in prediction and adaptation. The methodology has its ultimate usefulness in motor learning, thus the final aim has the goal of improving adaptive capabilities of cerebellar patients, which can have profound impact on rehabilitation programs.

Public Health Relevance

Impaired ability to make predictive movements, and to adaptive to changing conditions, can seriously impact health - especially if these largely automatic processes then require conscious processing. Impaired prediction adversely affects the ability to generate appropriate motor actions in anticipation of upcoming requirements, and impaired adaptation affects that ability to adjust for changes due to aging and disease. Procedures that train the brain to compensate for deficiencies in these areas can be of great benefit in programs of neural rehabilitation.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Exploratory/Developmental Grants (R21)
Project #
1R21EY019713-01A1
Application #
7895385
Study Section
Sensorimotor Integration Study Section (SMI)
Program Officer
Araj, Houmam H
Project Start
2010-05-01
Project End
2012-04-30
Budget Start
2010-05-01
Budget End
2011-04-30
Support Year
1
Fiscal Year
2010
Total Cost
$205,000
Indirect Cost
Name
Johns Hopkins University
Department
Otolaryngology
Type
Schools of Medicine
DUNS #
001910777
City
Baltimore
State
MD
Country
United States
Zip Code
21218
Wong, Aaron L; Shelhamer, Mark (2014) Similarities in error processing establish a link between saccade prediction at baseline and adaptation performance. J Neurophysiol 111:2084-93
Rine, Rosemarie M; Schubert, Michael C; Whitney, Susan L et al. (2013) Vestibular function assessment using the NIH Toolbox. Neurology 80:S25-31
Wong, Aaron L; Shelhamer, Mark (2013) A long-memory model of motor learning in the saccadic system: a regime-switching approach. Ann Biomed Eng 41:1613-24
Wong, Aaron L; Shelhamer, Mark (2012) Using prediction errors to drive saccade adaptation: the implicit double-step task. Exp Brain Res 222:55-64
Wong, Aaron L; Shelhamer, Mark (2011) Saccade adaptation improves in response to a gradually introduced stimulus perturbation. Neurosci Lett 500:207-11
Wong, Aaron L; Shelhamer, Mark (2011) Exploring the fundamental dynamics of error-based motor learning using a stationary predictive-saccade task. PLoS One 6:e25225
Wong, Aaron L; Shelhamer, Mark (2011) Sensorimotor adaptation error signals are derived from realistic predictions of movement outcomes. J Neurophysiol 105:1130-40