Paying attention to a sensory feature improves its perception and impairs that of others. Recent work has shown that a Normalization Model of Attention (NMoA) can account for a wide range of physiological findings and the influence of different attentional manipulations on visual performance. A key prediction of the NMoA is that attention to a visual feature like an orientation or a motion direction will increase the response of neurons preferring the attended feature (response gain) rather than increase the sensory input strength of the attended stimulus (input gain). This effect of feature-based attention on neuronal responses should translate to similar patterns of improvement in behavioral performance, with psychometric functions showing response gain rather than input gain when attention is directed to the task-relevant feature. In contrast, we report here that when human subjects are cued to attend to one of two motion directions in a transparent motion display, attentional effects manifest as a combination of input and response gain. Further, the impact on input gain is greater when attention is directed towards a narrow range of motion directions than when it is directed towards a broad range. These results are captured by an extended NMoA, which either includes a stimulus-independent attentional contribution to normalization or utilizes direction-tuned normalization. The proposed extensions are consistent with the feature-similarity gain model of attention and the attentional modulation in extrastriate area MT, where neuronal responses are enhanced and suppressed by attention to preferred and non-preferred motion directions respectively.

Attending to visual stimuli enhances the gain of those neurons in primate visual cortex that preferentially respond to the matching locations and features (on-target gain). Although this is well suited to enhance the neuronal representation of attended stimuli, it is nonoptimal under difficult discrimination conditions, as in the presence of similar distractors. In such cases, directing attention to neighboring neuronal populations (off-target gain) has been shown to be the most efficient strategy, but although such a strategic deployment of attention has been shown behaviorally, its underlying neural mechanisms are unknown. Here, we investigated how attention affects the population responses of neurons in the middle temporal (MT) visual area of rhesus monkeys to bidirectional movement inside the neurons’ receptive field (RF). The monkeys were trained to focus their attention onto the fixation spot or to detect a direction or speed change in one of the motion directions (the “target”), ignoring the distractor motion. Population activity profiles were determined by systematically varying the patterns’ directions while maintaining a constant angle between them. As expected, the response profiles show a peak for each of the 2 motion directions. Switching spatial attention from the fixation spot into the RF enhanced the peak representing the attended stimulus and suppressed the distractor representation. Importantly, the population data show a direction-dependent attentional modulation that does not peak at the target feature but rather along the slopes of the activity profile representing the target direction. Our results show that attentional gains are strategically deployed to optimize the discriminability of target stimuli, in line with an optimal gain mechanism proposed by Navalpakkam and Itti.

The lateral prefrontal cortex (lPFC) of primates is hypothesized to be heavily involved in decision-making and selective visual attention. Recent neurophysiological evidence suggests that information necessary for an orchestration of those high-level cognitive factors are indeed represented in the lPFC. However, we know little about the specific contribution of sub-networks within lPFC to the deployment of top-down influences that can be measured in extrastriate visual cortex. Here, we systematically applied electrical stimulations to areas 8Av and 45 of two macaque monkeys performing a concurrent goal-directed saccade task. Despite using currents well above saccadic thresholds of the directly adjacent Frontal Eye Fields (FEF), saccades were only rarely evoked by the stimulation. Instead, two types of behavioral effects were observed: Stimulations of caudal sites in 8Av (close to FEF) shortened or prolonged saccadic reaction times, depending on the task-instructed saccade, while rostral stimulations of 8Av/45 seem to affect the relative attentional weighting of saccade targets as well as saccadic reaction times. These results illuminate important differences in the causal involvement of different sub-networks within the lPFC and are most compatible with a stimulation-induced biasing of stimulus processing that accelerates the detection of saccade targets presented ipsilateral to stimulation through a disruption of contralaterally deployed top-down attention.