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. 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. Analysis of resting state functional magnetic resonance imaging (rsfMRI) showed that in the patient, relative to controls, two brain regions (right superior parietal lobule and right orbitofrontal cortex) that are normally connected to the resected area significantly increased their coupling with the areas homologue in the left hemisphere. Thus, in the absence of the right MFG, the left hemisphere homologue appears to have compensated (either during tumor growth or after resection) by increasing communication with other nodes of the visuospatial, decision-making and impulse control circuitry. We have also undertaken 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, we manipulated the attention field by affective valence (positive versus negative faces), while the stimulus size was 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 Naka-Rushton 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. A functional magnetic resonance imaging experiment confirmed that subjects attention fields were wider for positive faces than that for negative faces. Effective connectivity analysis showed that the emotional valence-dependent AF was closely associated with feedback from dorsolateral prefrontal cortex (DLPFC) to V1. Together, these findings suggest that emotional attention shapes perception by means of the normalization framework and that the DLPFC plays a crucial role in this process. 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 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.