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. The competition among multiple objects can be biased by both bottom-up sensory-driven mechanisms (exogenous attention), such as stimulus salience, and top-down, goal-directed influences, such as selective (endogenous) attention. 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. We previously reported that monkeys with lesions of prefrontal cortex (PFC) are impaired in their ability to switch top-down control. We then asked whether monkeys with these lesions would have altered single-unit responses in visual cortex as a result of a deprived source of attentional feedback from PFC. To answer this question, we surgically removed the entire lateral PFC in one hemisphere and transected the corpus callosum and anterior commissure in two macaques. This deprived visual cortex of PFC input in one hemisphere while keeping the other hemisphere intact. In the absence of PFC, attentional effects on neuronal responses and synchrony in area V4 of visual cortex (the site of recordings) were substantially reduced and the remaining effects of attention were delayed in time, indicating a critical role for PFC. Conversely, distracters captured attention and influenced V4 responses. However, because PFC lesions did not eliminate the effects of attention in V4, other sources of top-down attentional control signals to visual cortex must exist outside of PFC. Another possible source of top-down attentional control is the posterior parietal cortex. (PPC). Accordingly, we asked whether monkeys with PPC lesions would show similar or different behavioral effects as those with PFC lesions. Our results showed that, unlike monkeys with PFC lesions, those with PPC lesions were not selectively impaired in their ability to switch top-down control. Rather, they had a selective impairment in spatially locating targets they are required to discriminate. Thus, the PFC plays a critical role in the ability to switch attentional control on the basis of changing task demands, whereas the PPC plays a critical role in allocating attentional resources to behaviorally relevant spatial locations. Previous research has suggested that the right middle frontal gyrus (rMFG) may serve as a node of interaction between neural networks for top-down goal-directed endogenous attention and bottom-up, stimulus-driven exogenous attention. We tested this hypothesis by comparing the performance on an orientation discrimination task of a patient with a rMFG resection (to remove a brain tumor) and healthy controls. On endogenous attention trials, a valid central cue predicted with 90% accuracy the location of a peri-threshold Gabor patch. On the 10% invalid trials, the Gabor patch appeared in the opposite location to the cue. On exogenous attention trials, a cue appeared briefly at one of two peripheral locations, followed, after a variable inter-stimulus interval (ISI; range 0 to 700 ms), by a Gabor patch in either the same (valid) or opposite location (invalid). Analysis of behavioral data showed that for both patient and controls, valid cues facilitated faster reaction times compared to invalid cues, on endogenous and short ISI exogenous trials. However, at longer ISI exogenous trials, the patient was unable to withhold his responses, resulting in reduced performance compared to controls. This may be related to the patients inability to reorient attention in a top-down fashion after the effect of the exogenous cue has dissipated, and suggests a putative role of the rMFG in switching between exogenous and endogenous modes of attention. Resting state fMRI data revealed that the right superior parietal lobule and right orbitofrontal cortex showed significantly higher correlations with a left MFG seed region (a region tightly coupled with the right MFG in controls) in the patient relative to controls. We hypothesize that this paradoxical increase in cortical coupling represents a compensatory mechanism in the patient to offset the loss of function of the resected tissue in right prefrontal cortex. Finally, we have undertaken behavioral studies in healthy participants to explore the normalization model of attention, which proposes that attention can affect performance by contrast or response gain changes, depending on the stimulus size and the relative size of the attention field. Here, the attention field was manipulated by affective valence, namely, positive versus negative faces, while the stimulus size fixed in a spatial cueing task. Emotional faces served as a cue to attract spatial attention, followed by a pair of gratings. Subjects performed an orientation discrimination task on one of two gratings; for each of five contrasts (the contrasts of both gratings were identical on any given trial and co-varied across trials in random order). A response-cue at stimuli offset indicated the target location, yielding valid cues (the emotional face matched response-cue) and invalid cues (mismatched) conditions. Comparing performance accuracy (d') for valid and invalid trials revealed the spatial cueing effect for each contrast. The measured psychometric function for each affective valence (positive and negative) and each trial condition (valid and invalid) was fit with the standard NakaRushton equation. Two parameters d'max (asymptotic performance at high contrast levels) and c50 (the contrast yielding half maximum performance) determined response gain and contrast gain, respectively. We observed a change in the spatial cueing effect consonant with a change in contrast gain for positive faces and a change in response gain for negative faces. Significantly, individual differences in self-reported emotional strength of positive and negative faces correlated with contrast and response gain changes, respectively. An ongoing functional magnetic resonance imaging experiment confirmed that subjects attention fields were wider for positive faces than that for negative faces. Together, these findings suggest that emotional attention shapes perception by means of the normalization framework.

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35
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2015
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U.S. National Institute of Mental Health
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