Functional Anatomy of Perceptual and Attentional 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 objects 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 multiple objects 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. Classic theories of object-based attention (selection of one object in the context of competing distracters) assume a single object of selection but real-world tasks, such as driving a car, often require attending to multiple objects simultaneously. However, whether object-based attention can operate on more than one object at a time remains unexplored. Here, we used functional magnetic resonance imaging (fMRI) to address this question as human participants performed object-based attention tasks that required simultaneous attention to two objects differing in either their features or locations. Simultaneous attention to two objects differing in features (face and house) did not show significantly different responses in the fusiform face area (FFA) or parahippocampal place area (PPA), respectively, compared to attending a single object (face or house), but did enhance the response in the inferior frontal gyrus (IFG). Simultaneous attention to two circular arcs differing in locations did not show significantly different responses in the primary visual cortex (V1) compared to attending a single circular arc but did enhance the response in the intraparietal sulcus (IPS). These results suggest that object-based attention can simultaneously select at least two objects differing in their features or locations, processes mediated by the frontal and parietal cortex, respectively. Feature-based attention can influence responses to stimuli outside and contralateral to the attended location that share features with the attended stimulus, which demonstrates the spatially global effect of feature-based attention. However, how feature-based attention modulates neural responses in cortical areas from attended to unattended locations remains unclear. Here we used fMRI to investigate the underlying mechanism of this spatially global effect as human participants performed motion- (Experiment 1) and color- (Experiment 2) attention tasks. In Experiment 1, subjects were asked to attend one direction of motion within a display of overlapping upward and downward moving dots (the attended stimulus) on one side of a central fixation point, and ignore a single field of dots moving either up or down (the ignored stimulus) on the other side. In Experiment 2, the attended stimulus was comprised of overlapping fields of stationary red and green dots on one side of central fixation, and the ignored stimulus was a single field of red or green dots on the other side. Our results showed that, in both experiments, early visual, parietal, and prefrontal areas, as well as their respective sensory areas (MT+ for motion and V4 for color) all showed the classical feature-based attentional effect, with responses to the ignored stimulus significantly elevated when it shared the same feature as the attended stimulus. Using effective connectivity analysis, we found that the inferior frontal junction played a significant role in the spatially global effect of feature-based attention, indicating that this region is the neural substrate for the effect. Visuospatial attention often improves task performance by increasing signal gain at attended locations and decreasing noise at unattended locations. Attention is also believed to be the mechanism that allows information to enter awareness. In this behavioral experiment, we assessed whether orienting endogenous visuospatial attention with cues differentially affects visual discrimination sensitivity (an objective task performance) and visual awareness (the subjective feeling of perceiving) during the same discrimination task. Gabor patch targets were presented laterally, either at low contrast (contrast stimuli) or at high contrast embedded in noise (noise stimuli). Participants reported their orientation either in a 3-alternative choice task (clockwise, counterclockwise, unknown) that allowed for both objective and subjective reports, or in a 2-alternative choice task (clockwise, counterclockwise) that provided a control for objective reports. Signal detection theory models were fit to the experimental data: estimated perceptual sensitivity reflected objective performance; decision criteria, or subjective biases, were a proxy for visual awareness. Attention increased sensitivity (i.e., improved objective performance) for the contrast, but not for the noise stimuli. Indeed, with the latter, attention did not further enhance the already high target signal or reduce the already low uncertainty on its position. Interestingly, for both contrast and noise stimuli, attention resulted in more liberal criteria, i.e., awareness increased. The noise condition is thus an experimental configuration where people think they see the targets they attend to better, even if they do not. This could be explained by an internal representation of their attentional state, which influences awareness independent of objective visual signals. Finally, in this last project, fMRI data were acquired to explore the neural substrate of fine-grained awareness content and aimed to isolate it from well-known visual and attention networks. Here, the results showed that fronto-parietal and early visual areas in the human brain displayed a dichotomic pattern of activation, reflecting an ignition when participants become able to identify an image. A more gradual build-up of activation in parallel to the gradual identification of the images presented, was present in both the fronto-parietal network and along the ventra; visual pathway. Finally, the temporo-parietal junction appeared to be more active when participants are more confident of their choice (i.e., in identifying or not detecting an item). The results of this study help to clarify discrepancies in the literature by revealing how the neural correlates of consciousness depend on the specific question asked of the participant.