The Journal of Neurophysiology Vol. 80 No. 6 December 1998, pp. 2918-2940
Copyright ©1998 The American Physiological Society

Responses of Neurons in Inferior Temporal Cortex During Memory-Guided Visual Search

Leonardo Chelazzi^{1, 2}, John Duncan^{1, 3}, Earl K. Miller^{1, 4}, and Robert Desimone¹

¹ Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland 20892-4415; ² Dipartimento di Scienze Neurologiche e della Visione, Sezione di Fisiologia, University of Verona, Verona 37134, Italy; ³ Medical Research Council Applied Psychology Unit, Cambridge CB2 2EF, United Kingdom; ⁴ Department of Brain and Cognitive Sciences and The Center for Learning and Memory, MIT, Cambridge, Massachusetts 02139

Chelazzi, Leonardo, John Duncan, Earl K. Miller, and Robert Desimone. Responses of neurons in inferior temporal cortex during memory-guided visual search. J. Neurophysiol. 80: 2918-2940, 1998. A typical scene will contain many different objects, few of which are relevant to behavior at any given moment. Thus attentional mechanisms are needed to select relevant objects for visual processing and control over behavior. We examined this role of attention in the inferior temporal cortex of macaque monkeys, using a visual search paradigm. While the monkey maintained fixation, a cue stimulus was presented at the center of gaze, followed by a blank delay period. After the delay, an array of two to five choice stimuli was presented extrafoveally, and the monkey was rewarded for detecting a target stimulus matching the cue. The behavioral response was a saccadic eye movement to the target in one version of the task and a lever release in another. The array was composed of one "good" stimulus (effective in driving the cell when presented alone) and one or more "poor" stimuli (ineffective in driving the cell when presented alone). Most cells showed higher delay activity after a good stimulus used as the cue than after a poor stimulus. The baseline activity of cells was also higher preceding a good cue, if the animal expected it to occur. This activity may depend on a top-down bias in favor of cells coding the relevant stimulus. When the choice array was presented, most cells showed suppressive interactions between the stimuli as well as strong attention effects. When the choice array was presented in the contralateral visual field, most cells initially responded the same, regardless of which stimulus was the target. However, within 150-200 ms of array onset, responses were determined by the target stimulus. If the target was the good stimulus, the response to the array became equal to the response to the good stimulus presented alone. If the target was a poor stimulus, the response approached the response to that stimulus presented alone. Thus the influence of the nontarget stimulus was eliminated. These effects occurred well in advance of the behavioral response. When the array was positioned with stimuli on opposite sides of the vertical meridian, the contralateral stimulus appeared to dominate the response, and this dominant effect could not be overcome by attention. Overall, the results support a "biased competition" model of attention, according to which 1) objects in the visual field compete for representation in the cortex, and 2) this competition is biased in favor of the behaviorally relevant object by virtue of "top-down" feedback from structures involved in working memory.

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