Functional Anatomy Of Perceptual And Memory Systems In The Primate Brain

National Institute Of Mental Health

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Abstract

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.[unreadable] [unreadable] In the past year, we completed two studies aimed at understanding the role of prefrontal cortex in the control of attention. The first study examined which attentional functions are critically dependent on prefrontal cortex (PFC) by removing PFC unilaterally and transecting the forebrain commissures in two macaques. The monkeys fixated a central cue and discriminated the orientation of a colored target grating presented among colored distracter gratings in either the hemifield affected by the PFC lesion or the normal control hemifield. When the cue was held constant for many trials, task performance in the affected hemifield was nearly normal. However, performance was severely impaired when the cue was switched frequently across trials. The monkeys were unimpaired in a pop-out task with changing targets that did not require top-down attentional control. Thus, the PFC lesion resulted in selective impairment in the monkeys ability to switch top-down control. In the second study, we used fMRI to investigate the neural correlates of top-down control in humans performing tasks identical those used in the monkey experiments. Several fronto-parietal and posterior visual areas showed enhanced activation when attention was switched, which was greater on color cueing (top-down) trials relative to pop-out trials. Taken together, our findings indicate that both frontal and parietal cortices are involved in generating top-down control signals for attentive switching, which may then be fed back to visual processing areas. The PFC in particular plays a critical role in the ability to switch attentional control on the basis of changing task demands.