Reflexive and preparatory selection and suppression of salient information in the right and left posterior parietal cortex

Attentional cues can trigger activity in the parietal cortex in anticipation of visual displays, and this activity may, in turn, induce changes in other areas of the visual cortex, hence, implementing attentional selection. In a recent TMS study [Mevorach, C., Humphreys, G. W., & Shalev, L. Opposite biases in salience-based selection for the left and right posterior parietal cortex. Nature Neuroscience, 9, 740-742, 2006b], it was shown that the posterior parietal cortex (PPC) can utilize the relative saliency (a nonspatial property) of a target and a distractor to bias visual selection. Furthermore, selection was lateralized so that the right PPC is engaged when salient information must be selected and the left PPC when the salient information must be ignored. However, it is not clear how the PPC implements these complementary forms of selection. Here we used on-line triple-pulse TMS over the right or left PPC prior to or after the onset of global/local displays. When delivered after the onset of the display, TMS to the right PPC disrupted the selection of the more salient aspect of the hierarchical letter. In contrast, left PPC TMS delivered prior to the onset of the stimulus disrupted responses to the lower saliency stimulus. These findings suggest that selection and suppression of saliency, rather than being "two sides of the same coin," are fundamentally different processes. Selection of saliency seems to operate reflexively, whereas suppression of saliency relies on a preparatory phase that "sets up" the system in order to effectively ignore saliency

Functional brain organization of preparatory attentional control in visual search

Looking for an object that may be present in a cluttered visual display requires an advanced specification of that object to be created and then matched against the incoming visual input. Here, fast event-related fMRI was used to identify the brain networks that are active when preparing to search for a visual target. By isolating the preparation phase of the task it has been possible to show that for an identical stimulus, different patterns of cortical activation occur depending on whether participants anticipate a 'feature' or a 'conjunction' search task. When anticipating a conjunction search task, there was more robust activation in ventral occipital areas, new activity in the transverse occipital sulci and right posterior intraparietal sulcus. In addition, preparing for either type of search activated ventral striatum and lateral cerebellum. These results suggest that when participants anticipate a demanding search task, they develop a different advanced representation of a visually identical target stimulus compared to when they anticipate a nondemanding search. © 2013 Elsevier B.V. All rights reserved

The effects of TMS over dorsolateral prefrontal cortex on multiple visual object memory across fixation and saccades

Trans-saccadic memory, the process by which the visual system maintains the spatial position and features of objects across eye movements, is thought to be a form of visual working memory (Irwin, 1991). It has been shown that TMS over the frontal and parietal eye fields degrades trans-saccadic memory of multiple object features (Prime et al., 2008, 2010). We used a similar TMS protocol to investigate whether dorsolateral prefrontal cortex (DLPFC) is also involved in trans-saccadic memory. We predicted that performance would be disrupted similarly during either fixation or saccades. Instead, we found both task and hemisphere-dependent effects. During fixation, TMS over left DLPFC produced inconsistent effects, whereas TMS over right DLPFC reduced performance, consistent with its known role in working memory (Goldman-Rakic, 1987). In contrast, TMS over both sides of DLPFC enhanced trans-saccadic memory, suggesting a dis-inhibition of trans-saccadic processing. These results suggest that visual working memory during fixation and trans-saccadic memory may be supported by different, but interacting, neural circuits

Pre-Stimulus Activity Predicts the Winner of Top-Down vs. Bottom-Up Attentional Selection

Our ability to process visual information is fundamentally limited. This leads to competition between sensory information that is relevant for top-down goals and sensory information that is perceptually salient, but task-irrelevant. The aim of the present study was to identify, from EEG recordings, pre-stimulus and pre-saccadic neural activity that could predict whether top-down or bottom-up processes would win the competition for attention on a trial-by-trial basis. We employed a visual search paradigm in which a lateralized low contrast target appeared alone, or with a low (i.e., non-salient) or high contrast (i.e., salient) distractor. Trials with a salient distractor were of primary interest due to the strong competition between top-down knowledge and bottom-up attentional capture. Our results demonstrated that 1) in the 1-sec pre-stimulus interval, frontal alpha (8–12 Hz) activity was higher on trials where the salient distractor captured attention and the first saccade (bottom-up win); and 2) there was a transient pre-saccadic increase in posterior-parietal alpha (7–8 Hz) activity on trials where the first saccade went to the target (top-down win). We propose that the high frontal alpha reflects a disengagement of attentional control whereas the transient posterior alpha time-locked to the saccade indicates sensory inhibition of the salient distractor and suppression of bottom-up oculomotor capture

The role of the lateral prefrontal cortex and anterior cingulate in stimulus–response association reversals

Many complex tasks require us to flexibly switch between behavioral rules, associations, and strategies. The prefrontal cerebral cortex is thought to be critical to the performance of such behaviors, although the relative contribution of different components of this structure and associated subcortical regions are not fully understood. We used functional magnetic resonance imaging to measure brain activity during a simple task which required repeated reversals of a rule linking a colored cue and a left/right motor response. Each trial comprised three discrete events separated by variable delay periods. A colored cue instructed which response was to be executed, followed by a go signal which told the subject to execute the response and a feedback instruction which indicated whether to ‘‘hold’’ or ‘‘f lip’’ the rule linking the colored cue and response. The design allowed us to determine which brain regions were recruited by the specific demands of preparing a rule contingent motor response, executing such a response, evaluating the significance of the feedback, and reconfiguring stimulus–response (SR) associations. The results indicate that an increase in neural activity occurs within the anterior cingulate gyrus under conditions in which SR associations are labile. In contrast, lateral frontal regions are activated by unlikely/unexpected perceptual events regardless of their significance for behavior. A network of subcortical structures, including the mediodorsal nucleus of the thalamus and striatum were the only regions showing activity that was exclusively correlated with the neurocognitive demands of reversing SR associations. We conclude that lateral frontal regions act to evaluate the behavioral significance of perceptual events, whereas medial frontal–thalamic circuits are involved in monitoring and reconfiguring SR associations when necessary

Frontoparietal networks underlying saccadic eye movements in the common marmoset

Common marmosets (Callithrix jacchus) are small-bodied New World primates that are increasingly popular as model animals for neuroscience research. Their lissencephalic cortex provides substantial advantages for the application of high-density electrophysiological techniques to enhance our understanding of local cortical circuits and their cognitive and motor functions. The oculomotor circuitry underlying saccadic eye movements has been a popular system to study cognitive control. Most of what we know about this system, comes from electrophysiological studies on macaques, but most of their cortical oculomotor areas are buried within sulci and harder to access for high-density recordings. In contrast, marmosets provide greater advantages for studies of the oculomotor system, since critical areas of this network such as the frontal eye fields (FEF) and lateral intraparietal area (LIP) are easily accessible at the cortical surface. In contrast to the well-established macaques, little is known about functional connectivity patterns of common marmosets. In this thesis, we used resting-state ultra-high-field fMRI on anesthetized marmosets and macaques along with awake human subjects, to examine and compare the functional organization of the brain, with emphasis on the saccade system. Independent component analysis revealed homologous resting-state networks in marmoset to those in macaques and humans, including a distributed frontoparietal network. Seed-region analyses of the marmoset superior colliculus (SC) revealed the strongest frontal functional connectivity with area 8aD bordering area 6DR. This frontal region exhibited a similar functional connectivity pattern to the FEF in macaques and humans. The results supported an evolutionarily preserved frontoparietal system and provided a starting point for invasive neurophysiological studies in the marmoset saccade system. We started by investigating the function of the marmoset posterior parietal cortex with electrical microstimulation. We implanted 32-channel Utah arrays at the location of area LIP as identified from our resting-state fMRI study and applied microstimulation while animals watched videos. Similar to macaque studies, stimulation evoked fixed-vector and goal-directed saccades, staircase saccades, and eyeblinks in marmosets. These findings demonstrated that the marmoset area LIP plays a role in the regulation of eye movements and is potentially homologous to that of the macaque. Next, we recorded the neuronal activity in marmoset areas LIP and 8aD using linear electrode arrays while animals performed a pro/antisaccade task. The antisaccade task is a popular paradigm to probe executive control. In this task, participants suppress a prepotent stimulus-driven response in favor of a less potent response away from the stimulus. Our behavioral findings indicated that area 8aD neurons were significantly more active for correct than errorenous antisaccades in contralateral directions, with respect to the recording site. We found neurons with significant stimulus-related activity in area LIP and significant saccade-related neurons in both areas 8aD and LIP. These findings provided further evidence on the role of marmoset frontal and parietal oculomotor areas in oculomotor control, supporting marmosets as alternative primate models of the oculomotor system

Cross-modal orienting of exogenous attention results in visual-cortical facilitation, not suppression

Attention may be oriented exogenously (i.e., involuntarily) to the location of salient stimuli, resulting in improved perception. However, it is unknown whether exogenous attention improves perception by facilitating processing of attended information, suppressing processing of unattended information, or both. To test this question, we measured behavioral performance and cue-elicited neural changes in the electroencephalogram as participants (N = 19) performed a task in which a spatially non-predictive auditory cue preceded a visual target. Critically, this cue was either presented at a peripheral target location or from the center of the screen, allowing us to isolate spatially specific attentional activity. We find that both behavior and attention-mediated changes in visual-cortical activity are enhanced at the location of a cue prior to the onset of a target, but that behavior and neural activity at an unattended target location is equivalent to that following a central cue that does not direct attention (i.e., baseline). These results suggest that exogenous attention operates via facilitation of information at an attended location

Incentive Processing and Inhibitory Control in Adolescents and Young Adults

Adolescents are known to demonstrate normative increases in risk-taking behaviors. Understanding the interaction between incentive (reward, punishment) processing and basic cognitive control abilities, both of which are still maturing into adolescence, may provide insight on the basic mechanisms contributing to this complex behavioral phenomenon. In this dissertation, we present a compilation of papers aimed at characterizing the influence of potential reward gain or loss on response inhibition performance and supporting brain circuitry in adolescents and adults. In study 1, we use fast, event-related functional magnetic resonance imaging (fMRI) to examine the neural circuitry supporting perfomance on an antisaccade task with reward or neutral contingencies added to each trial. Results indicate that components of the adolescent reward system exhibit an initially sluggish, then eventually overactive response to rewards, as well as limited recruitment in regions supporting the executive assessment of rewards. In study 2, the effects of different magnitudes of potential gains and losses on antisaccade task performance were examined. Results indicate that higher compared to lower magnitude reward contingencies differentially affect adolescent, but not adult, response suppression abilities. Furthemore, both age groups performed consistently well (low error rates) on punishment trials. In study 3, adolescents and adults underwent fast, event-related fMRI as they performed a rewarded antisaccade task with fixed-magnitude reward and punishment stimuli, previously determined to result in equivalent levels of behavioral performance across the age groups (study 2). Additionally, auditory, performance-based feedback was provided on each trial. fMRI results indicate that during detection of reward cues, adolescents do not show the same early recruitment of oculomotor control regions evident in adults. Furthermore, adolescents demonstrated temporally extended responses in several brain regions (e.g., orbitofrontal cortex, supplementary eye field) during the preparatory period of potential punishment trials, reflecting possible immaturities in mechanisms underlying potential loss or 'risk' anticipation. Finally, adults demonstrated enhanced activity in the ventral striatum and cortical eye fields during the response/feedback epoch, suggesting more mature consummatory processing. Collectively, the results of these studies demonstrate protracted development of higher-order executive aspects of reward processing and its interaction with response inhibition abilites into adolescence

Age-related differences in selection by visual saliency

We examined the ability of older adults to select local and global stimuli varying in perceptual saliency – a task requiring non-spatial visual selection. Participants were asked to identify in separate blocks a target at either the global or local level of a hierarchical stimulus, while the saliency of each level was varied (across different conditions either the local or the global form was the more salient and relatively easier to identify). Older adults were less efficient than young adults in ignoring distractors that were higher in saliency than targets, and this occurred across both the global and local levels of form. The increased effects of distractor saliency on older adults occurred even when the effects were scaled by overall differences in task performance. The data provide evidence for an age-related decline in non spatial attentional selection of low-salient hierarchical stimuli, not determined by the (global or local) level at which selection was required. We discuss the implications of these results for understanding both the interaction between saliency and hierarchical processing and the effects of aging on non-spatial visual attention