Motor adaptation refines our movements during development, adjusts them when we attempt to acquire a new skill, and repairs them if they are compromised by injury. Our long-term goal is to identify the neural mechanisms of the motor adaptation that maintains the accuracy of saccadic eye movements. Most, if not all, neurophysiological studies on saccade adaptation have used targeting (reactive) saccades made in response to the sudden appearance of a target that falls off the fovea, called here the retinotopic goal of the saccade. For targeting saccades, the vectors of the retinotopic goal and the initial motor error (the difference between the target and current eye positions [also called the desired saccade vector]) are congruent. However, saccades often must be coordinated with other saccades or other types of eye movement, which may intervene before a saccade to an intended goal is executed. Such interruptions dissociate the vector of the saccade to be executed and its retinotopic goal, so the brain must perform a spatial updating to re-compute the vector of the intended saccade. Our preliminary experiments using a double-saccade task (DST) revealed that (1) the saccadic burst of saccade-related neurons in the superior colliculus (SC) are modulated by the retinotopic goal, and (2) unexpectedly, adaptation of targeting saccades does not generalize i.e., transfer, to the second saccade of a DST, even when the two saccades have identical initial motor errors. These findings lead us to hypothesize that the SC uses different processing for targeting saccades and saccades that require spatial updating. We will examine the effect of this separate processing on saccade adaptation. We will use three approaches to test this hypothesis: 1. Behavioral experiments to infer the adaptation sites of targeting saccades and the second saccade of a DST on the basis of both the characteristics of each adaptation and its transfer to the other type of saccade. 2. single unit recording to reveal any changes in SC activity specific to the two different saccade types and their adaptations and 3. microstimulation and focal inactivation to test the difference of SC topographic activity during the execution of saccades in the two tasks . Because of the similarities of simian and human saccadic eye movement behavior, the results of this project should have considerable relevance in the diagnosis, treatment and rehabilitation of patients with saccadic eye movement disorders. Our proposed experiments aim to provide both behavioral and neurophysiological evidence that adaptation of saccades with the same vectors, but generated in different goal contexts, do not transfer to each other and hence involve different adaptation pathways. Understanding the limitation of the transfer of adaptation between saccades in different contexts may help to design a more specific repertoire of rehabilitation strategies for patients with saccade disorders, and perhaps general motor deficits.

Public Health Relevance

This proposal studies the brain mechanisms of adaptation of saccadic eye movement that keep the eye movement accurate which is critical to normal vision. We will investigate different neuronal pathways that serve adaptation of saccadic eye movements in different behavioral contexts. The results of this project are relevance in the diagnostics, treatment and rehabilitation of patients with saccadic eye movement disorders.

National Institute of Health (NIH)
National Eye Institute (NEI)
Research Project (R01)
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Mechanisms of Sensory, Perceptual, and Cognitive Processes Study Section (SPC)
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Araj, Houmam H
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University of Washington
Schools of Medicine
United States
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Kojima, Yoshiko; Soetedjo, Robijanto (2018) Elimination of the error signal in the superior colliculus impairs saccade motor learning. Proc Natl Acad Sci U S A 115:E8987-E8995
Soetedjo, Robijanto (2018) Signals driving the adaptation of saccades that require spatial updating. J Neurophysiol 120:525-538
Herzfeld, David J; Kojima, Yoshiko; Soetedjo, Robijanto et al. (2018) Encoding of error and learning to correct that error by the Purkinje cells of the cerebellum. Nat Neurosci 21:736-743
Kojima, Yoshiko; Soetedjo, Robijanto (2017) Selective reward affects the rate of saccade adaptation. Neuroscience 355:113-125
Galvan, Adriana; Stauffer, William R; Acker, Leah et al. (2017) Nonhuman Primate Optogenetics: Recent Advances and Future Directions. J Neurosci 37:10894-10903
Kojima, Yoshiko; Soetedjo, Robijanto (2017) Change in sensitivity to visual error in superior colliculus during saccade adaptation. Sci Rep 7:9566
El-Shamayleh, Yasmine; Kojima, Yoshiko; Soetedjo, Robijanto et al. (2017) Selective Optogenetic Control of Purkinje Cells in Monkey Cerebellum. Neuron 95:51-62.e4
Herzfeld, David J; Kojima, Yoshiko; Soetedjo, Robijanto et al. (2015) Encoding of action by the Purkinje cells of the cerebellum. Nature 526:439-42
Kojima, Yoshiko; Fuchs, Albert F; Soetedjo, Robijanto (2015) Adaptation and adaptation transfer characteristics of five different saccade types in the monkey. J Neurophysiol 114:125-37
Kojima, Yoshiko; Robinson, Farrel R; Soetedjo, Robijanto (2014) Cerebellar fastigial nucleus influence on ipsilateral abducens activity during saccades. J Neurophysiol 111:1553-63

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