When one chooses to look at something, one makes a saccadic eye movement to it. Because saccades are so brief, they cannot be guided by visual feedback, but must rely on feedback after each saccade to check the accuracy of that movement and, if needed, to adjust subsequent saccades;this is saccade adaptation. Although the specific mechanisms underlying saccadic adaptation are largely unknown, it is generally inferred that saccades are recalibrated depending on the retinal error after each saccade, i.e., the distance of the fovea from the target of the saccade. In the laboratory, saccade adaptation is induced by consistently and surreptitiously moving the target during each saccade (when vision is poor), with the result that the oculomotor system compensates as though its saccades had been in error. We propose to explore whether saccade adaptation is best described in engineering terms as a servo mechanism that reduces an error signal, or in behaviorist terms as an example of motor learning driven by reinforcement. We propose to compare two forms of saccade adaptation: (a) that produced conventionally by moving the target during the saccade, and (b) that produced by rewarding subjects for making saccades of a particular magnitude without the target being present after the saccade. Specifically, we propose to see how similar the two forms of adaptation are by comparing the temporal parameters known to affect the efficacy of conventional saccade adaptation (for example, delaying the feedback after each saccade). Furthermore, we propose a test that delineates a crucial difference between a system guided by error and one guided by reinforcement: is adaptation more effective if the subject only receives feedback on trials that land directly on the target versus trials that do not (and therefore present a visual error)? The conventional servo theory would predict that only the latter type of trials would be effective;the reinforcement theory would predict that the former one would be effective. We also propose to look for natural visual features that might act as natural reinforcers for saccades (image contrast, sharpness or duration). Finally, because saccade characteristics are modulated by basal ganglia activity, and reinforcement-guided adaptation would almost certainly involve the basal ganglia, and because patients with Parkinson's Disease have damage in this area and show deficits in other forms of motor learning, we propose to study saccade adaptation in Parkinson's patients, in collaboration with Felice Ghilardi of the CUNY Medical School.

Public Health Relevance

of this proposal rests on two issues: First, a part of this proposal concerns the study of the deficits of patients with Parkinson's disease. This pathology is the most common neurodegenerative disorder after Alzheimer's disease, with prevalence predicted to rise to 610,000 by 2030. Understanding this pathology is an urgent matter of public health. Abnormal saccadic eye-movements (staircase patterns) have been identified as a sensitive and specific biomarker for Parkinson's disease patients as well as a subset of patients at-risk. A better understanding of the Parkinson's phenotype may lead more efficient diagnostic and rehabilitation techniques for the patients. Second, given that the metrics of saccades appear to be influenced by reinforcement, we can presume that other specific oculomotor deficiencies may also be manifestations of more general deficits in learning or attention. For example, schizophrenic patients are well known to show low gains of smooth pursuit eye movements. Unpublished work by the one of our key persons, Laurent Madelain, has shown that the gain of these patients can be readily raised to normal levels by giving explicit reinforcement for high-gain pursuit.

National Institute of Health (NIH)
National Eye Institute (NEI)
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Central Visual Processing Study Section (CVP)
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Araj, Houmam H
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City College of New York
Schools of Arts and Sciences
New York
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Azadi, Reza; Harwood, Mark R (2014) Visual cues that are effective for contextual saccade adaptation. J Neurophysiol 111:2307-19
Gray, Michael J; Blangero, Annabelle; Herman, James P et al. (2014) Adaptation of naturally paced saccades. J Neurophysiol 111:2343-54
Madelain, Laurent; Herman, James P; Harwood, Mark R (2013) Saccade adaptation goes for the goal. J Vis 13:
Herman, James P; Cloud, C Phillip; Wallman, Josh (2013) End-point variability is not noise in saccade adaptation. PLoS One 8:e59731
Herman, James P; Blangero, Annabelle; Madelain, Laurent et al. (2013) Saccade adaptation as a model of flexible and general motor learning. Exp Eye Res 114:6-15
Belyusar, Daniel; Snyder, Adam C; Frey, Hans-Peter et al. (2013) Oscillatory alpha-band suppression mechanisms during the rapid attentional shifts required to perform an anti-saccade task. Neuroimage 65:395-407
Collins, Therese; Wallman, Josh (2012) The relative importance of retinal error and prediction in saccadic adaptation. J Neurophysiol 107:3342-8
Paeye, Celine; Madelain, Laurent (2011) Reinforcing saccadic amplitude variability. J Exp Anal Behav 95:149-62
Madelain, Laurent; Paeye, Celine; Wallman, Josh (2011) Modification of saccadic gain by reinforcement. J Neurophysiol 106:219-32
Madelain, Laurent; Paeye, Celine; Darcheville, Jean-Claude (2011) Operant control of human eye movements. Behav Processes 87:142-8

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