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The Journal of Neuroscience, February 18, 2009, 29(7):2136-2150; doi:10.1523/JNEUROSCI.3962-08.2009

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Behavioral/Systems/Cognitive
Correlates of Perceptual Learning in an Oculomotor Decision Variable

Patrick M. Connolly, Sharath Bennur, and Joshua I. Gold

Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104

Correspondence should be addressed to Joshua I. Gold, University of Pennsylvania, Department of Neuroscience, 116 Johnson Pavilion, 3610 Hamilton Walk, Philadelphia, PA 19104-6074. Email: jigold{at}mail.med.upenn.edu

In subjects trained extensively to indicate a perceptual decision with an action, neural commands that generate the action can represent the process of forming the decision. However, it is unknown whether this representation requires overtraining or reflects a more general link between perceptual and motor processing. We examined how perceptual processing is represented in motor commands in naive monkeys being trained on a demanding perceptual task, as they first establish the sensory–motor association and then learn to form more accurate perceptual judgments. The task required the monkeys to decide the direction of random-dot motion and respond with an eye movement to one of two visual targets. Using electrically evoked saccades, we examined oculomotor commands that developed during motion viewing. Throughout training, these commands tended to reflect both the subsequent binary choice of saccade target and the weighing of graded motion evidence used to arrive at that choice. Moreover, these decision-related oculomotor signals, along with the time needed to initiate the voluntary saccadic response, changed steadily as training progressed, approximately matching concomitant improvements in behavioral sensitivity to the motion stimulus. Thus, motor circuits may have general access to perceptual processing used to select between actions, even without extensive training. The results also suggest a novel candidate mechanism for some forms of perceptual learning, in which the brain learns rapidly to treat a perceptual decision as a problem of action selection and then over time to use sensory input more effectively to guide the selection process.

Key words: perceptual learning; decision; microstimulation; frontal eye field; saccade; oculomotor

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Received Aug. 20, 2008; revised Jan. 9, 2009; accepted Jan. 13, 2009.

Correspondence should be addressed to Joshua I. Gold, University of Pennsylvania, Department of Neuroscience, 116 Johnson Pavilion, 3610 Hamilton Walk, Philadelphia, PA 19104-6074. Email: jigold{at}mail.med.upenn.edu

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