Functional Anatomy Of Perceptual And Memory Systems In The Primate Brain

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A typical scene contains many different objects that compete for neural representation due to the limited processing capacity of the visual system. At the neural level, competition among multiple stimuli is evidenced by the mutual suppression of their visually evoked responses and occurs most strongly at the level of the receptive field. The competition among multiple objects can be biased by both bottom-up sensory-driven mechanisms and top-down influences, such as selective attention. Functional brain imaging studies reveal that biasing signals due to selective attention can modulate neural activity in visual cortex not only in the presence but also in the absence of visual stimulation. Although the competition among stimuli for representation is ultimately resolved within visual cortex, the source of top-down biasing signals likely derives from a distributed network of areas in frontal and parietal cortex. This biased competition model of attention suggests that once attentional resources are depleted, no further processing is possible. Yet, existing data suggest that emotional stimuli activate brain regions "automatically," largely immune from attentional control. We tested the alternative possibility, namely, that the neural processing of stimuli with emotional content is not automatic and instead requires some degree of attention. Our results revealed that, contrary to the prevailing view, all brain regions responding differentially to emotional faces, including the amygdala, did so only when sufficient attentional resources were available to process the faces. Thus, similar to the processing of other stimulus categories, the processing of facial expression is under top-down control. In our work completed during the past year, we have examined the specific contributions made by prefrontal cortex to the top-down control of visual attention. We prepared monkeys with unilateral lesions of the prefrontal cortex in combination with transection of the forebrain commissures. As a result, visual processing could be modulated by prefrontal feedback in only one hemisphere. Monkeys were trained to fixate a central spot and discriminate the orientation of a colored target grating presented among colored distracters in either the control hemifield or the hemifield affected by the PFC lesion. The location of the stimuli was varied, and the color of a central cue specified the color of the target on each trial. The critical component of this task was that the specific target grating on one trial might be a distracter on the next. When the cue was held constant for many trials, the monkeys were nearly normal (as measured by orientation thresholds) in using top-down mechanisms to guide attention to the target location. However, the monkeys were severely impaired when the cue was switched frequently across trials (5 trials or less in a block). An analysis of errors indicated that on trials in which the cue changed color, animals frequently continued to incorrectly apply the cue information from the immediately preceding trial, or trials. The monkeys were not impaired in a pop-out task with changing targets that did not require top-down attentional control. This suggest that prefrontal cortex plays a critical role when animals must flexibly reallocate attention on the basis of changing information and task demands from one moment to the next. The results may also help explain perseveration seen in patients with frontal lobe damage.