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J Neurophysiol (January 7, 2004). doi:10.1152/jn.00872.2003
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Submitted on September 8, 2003
Accepted on December 25, 2003

Representation of an Abstract Perceptual Decision in Macaque Superior Colliculus

Gregory D. Horwitz1*, Aaron P. Batista1, and William T. Newsome1

1 Howard Hughes Medical Institute, Stanford, CA, USA; Neurobiology, Stanford University School of Medicine, Stanford, CA, USA

* To whom correspondence should be addressed. E-mail: horwitz{at}salk.edu.

We recorded from neurons in the intermediate and deep layers of the superior colliculus (SC) while monkeys performed a novel direction discrimination task. In contrast to the task we have used previously, the new version required the monkey to dissociate perceptual judgments from preparation to execute specific operant saccades. The monkey discriminated between two opposed directions of motion in a random dot motion stimulus and was required to maintain the decision in memory throughout a delay period before the target of the required operant saccade was revealed. We hypothesized that perceptual decisions made in this paradigm would be represented in an "abstract" or "categorical" form within the brain, probably in frontal cortex, and that decision-related neural activity would be eliminated from spatially organized preoculomotor structures such as the SC. To our surprise, however, a small population of neurons in the intermediate and deep layers of the SC fired in a choice-specific manner early in the trial well before the monkey could plan the operant saccade. Furthermore, the representation of the decision during the delay period appeared to be spatial: the active region in the SC map corresponded to the region of space toward which the perceptually discriminated stimulus motion flowed. Electrical microstimulation experiments suggested that these decision-related SC signals were not merely related to covert saccade planning. We conclude that monkeys may employ, in part, a spatially-referenced mnemonic strategy for representing perceptual decisions, even when an abstract, categorical representation might appear more likely a priori.




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