Top-Down Biasing of Visual Cortical Activity Encodes Attended Information and Facilitates Behavioral Performance in Visual Spatial Attention.

Top-down attention plays a vital role in selecting relevant stimuli and suppressing distracting information. During top-down visual-spatial attention, control signals from the dorsal attention network modulate the baseline neuronal activity in the visual cortex in favor of task-relevant stimuli. While several studies have demonstrated that baseline shift during anticipatory attention occurs in multiple visual areas, such effects have not been systematically investigated across the visual hierarchy, especially when different attention conditions are matched for stimulus and task factors. In this fMRI study, we investigated anticipatory attention signals using univariate and multivariate (MVPA) analysis in multiple visual cortical areas. First, the univariate analysis yielded significant activation differences in higher-order visual areas, with the effect weaker in early visual areas. Second, however, in contrast, MVPA decoding was significant in predicting attention conditions in all visual areas and IPS, with lower-order visual areas (e.g., V1) having greater decoding accuracy than higher-order visual areas (e.g., LO1). Third, the strength of decoding accuracy predicted the behavioral performance in the discrimination task. All the results were highly replicable and consistent across two datasets with same experimental paradigms but recorded at two research sites, and two experimental conditions where the direction of spatial attention was driven either by external instructions (cue-instructed attention) or from internal decisions (free-choice attention). Our results provide clear evidence, not available in past univariate investigations, that top-down attentional control signals selectively bias neuronal processing throughout the visual hierarchy, and that this biasing is correlated with the task performance.

Top-down control of the left visual field bias in cued visual spatial attention.

A left visual field (LVF) bias in perceptual judgments, response speed, and discrimination accuracy has been reported in humans. Cognitive factors, such as visual spatial attention, are known to modulate or even eliminate this bias. We investigated this problem by recording pupillometry together with functional magnetic resonance imaging (fMRI) in a cued visual spatial attention task. We observed that (i) the pupil was significantly more dilated following attend-right than attend-left cues, (ii) the task performance (e.g. reaction time [RT]) did not differ between attend-left and attend-right trials, and (iii) the difference in cue-related pupil dilation between attend-left and attend-right trials was inversely related to the corresponding difference in RT. Neuroscientically, correlating the difference in cue-related pupil dilation with the corresponding cue-related fMRI difference yielded activations primarily in the right hemisphere, including the right intraparietal sulcus and the right ventrolateral prefrontal cortex. These results suggest that (i) there is an asymmetry in visual spatial attention control, with the rightward attention control being more effortful than the leftward attention control, (ii) this asymmetry underlies the reduction or the elimination of the LVF bias, and (iii) the components of the attentional control networks in the right hemisphere are likely part of the neural substrate of the observed asymmetry in attentional control.

Role of Inferior Frontal Junction (IFJ) in the Control of Feature versus Spatial Attention.

Feature-based visual attention refers to preferential selection and processing of visual stimuli based on their nonspatial attributes, such as color or shape. Recent studies have highlighted the inferior frontal junction (IFJ) as a control region for feature but not spatial attention. However, the extent to which IFJ contributes to spatial versus feature attention control remains a topic of debate. We investigated in humans of both sexes the role of IFJ in the control of feature versus spatial attention in a cued visual spatial (attend-left or attend-right) and feature (attend-red or attend-green) attention task using fMRI. Analyzing cue-related fMRI using both univariate activation and multivoxel pattern analysis, we found the following results in IFJ. First, in line with some prior studies, the univariate activations were not different between feature and spatial attentional control. Second, in contrast, the multivoxel pattern analysis decoding accuracy was above chance level for feature attention (attend-red vs attend-green) but not for spatial attention (attend-left vs attend-right). Third, while the decoding accuracy for feature attention was above chance level during attentional control in the cue-to-target interval, it was not during target processing. Fourth, the right IFJ and visual cortex (V4) were observed to be functionally connected during feature but not during spatial attention control, and this functional connectivity was positively associated with subsequent attentional selection of targets in V4, as well as with behavioral performance. These results support a model in which IFJ plays a crucial role in top-down control of visual feature but not visual spatial attention.SIGNIFICANCE STATEMENT Past work has shown that the inferior frontal junction (IFJ), a prefrontal structure, is activated by both attention-to-feature (e.g., color) and attention-to-location, but the precise role of IFJ in the control of feature- versus spatial-attention is debated. We investigated this issue in a cued visual spatial (attend-left or attend-right) and feature (attend-red or attend-green) attention task using fMRI, multivoxel pattern analysis, and functional connectivity methods. The results show that (1) attend-red versus attend-green can be decoded in single-trial cue-evoked BOLD activity in IFJ but not attend-left versus attend-right and (2) only right IFJ modulates V4 to enhance task performance. This study sheds light on the function and hemispheric specialization of IFJ in the control of visual attention.

The Microstructure of Attentional Control in the Dorsal Attention Network.

The top-down control of attention involves command signals arising chiefly in the dorsal attention network (DAN) in frontal and parietal cortex and propagating to sensory cortex to enable the selective processing of incoming stimuli based on their behavioral relevance. Consistent with this view, the DAN is active during preparatory (anticipatory) attention for relevant events and objects, which, in vision, may be defined by different stimulus attributes including their spatial location, color, motion, or form. How this network is organized to support different forms of preparatory attention to different stimulus attributes remains unclear. We propose that, within the DAN, there exist functional microstructures (patterns of activity) specific for controlling attention based on the specific information to be attended. To test this, we contrasted preparatory attention to stimulus location (spatial attention) and to stimulus color (feature attention), and used multivoxel pattern analysis to characterize the corresponding patterns of activity within the DAN. We observed different multivoxel patterns of BOLD activation within the DAN for the control of spatial attention (attending left vs. right) and feature attention (attending red vs. green). These patterns of activity for spatial and feature attentional control showed limited overlap with each other within the DAN. Our findings thus support a model in which the DAN has different functional microstructures for distinctive forms of top-down control of visual attention.

Working Memory Capacity Is Negatively Associated with Memory Load Modulation of Alpha Oscillations in Retention of Verbal Working Memory.

Working memory capacity (WMC) measures the amount of information that can be maintained online in the face of distraction. Past work has shown that the efficiency with which the frontostriatal circuit filters out task-irrelevant distracting information is positively correlated with WMC. Recent work has demonstrated a role of posterior alpha oscillations (8-13 Hz) in providing a sensory gating mechanism. We investigated the relationship between memory load modulation of alpha power and WMC in two verbal working memory experiments. In both experiments, we found that posterior alpha power increased with memory load during memory, in agreement with previous reports. Across individuals, the degree of alpha power modulation by memory load was negatively associated with WMC, namely, the higher the WMC, the less alpha power was modulated by memory load. After the administration of topiramate, a drug known to affect alpha oscillations and have a negative impact on working memory function, the negative correlation between memory load modulation of alpha power and WMC was no longer statistically significant but still somewhat detectable. These results suggest that (1) individuals with low WMC demonstrate stronger alpha power modulation by memory load, reflecting possibly an increased reliance on sensory gating to suppress task-irrelevant information in these individuals, in contrast to their high WMC counterparts who rely more on frontal areas to perform this function and (2) this negative association between memory load modulation of alpha oscillations and WMC is vulnerable to drug-related cognitive disruption.

Neural mechanisms of internal distraction suppression in visual attention.

When performing a demanding cognitive task, internal distraction in the form of task-irrelevant thoughts and mind wandering can shift our attention away from the task, negatively affecting task performance. Behaviorally, individuals with higher executive function indexed by higher working memory capacity (WMC) exhibit less mind wandering during cognitive tasks, but the underlying neural mechanisms are unknown. To address this problem, we recorded functional magnetic resonance imaging (fMRI) data from subjects performing a cued visual attention task, and assessed their WMC in a separate experiment. Applying machine learning and time-series analysis techniques, we showed that (1) higher WMC individuals experienced lower internal distraction through stronger suppression of posterior cingulate cortex (PCC) activity, (2) higher WMC individuals had better neural representations of attended information as evidenced by higher multivoxel decoding accuracy of cue-related activities in the dorsal attention network (DAN), (3) the positive relationship between WMC and DAN decoding accuracy was mediated by suppression of PCC activity, (4) the dorsal anterior cingulate (dACC) was a source of top-down signals that regulate PCC activity as evidenced by the negative association between Granger-causal influence dACC→PCC and PCC activity levels, and (5) higher WMC individuals exhibiting stronger dACC→PCC Granger-causal influence. These results shed light on the neural mechanisms underlying the executive suppression of internal distraction in tasks requiring externally oriented attention and provide an explanation of the individual differences in such suppression.

Theta Oscillations Index Frontal Decision-Making and Mediate Reciprocal Frontal-Parietal Interactions in Willed Attention.

Attention can be attracted reflexively by sensory signals, biased by learning or reward, or focused voluntarily based on momentary goals. When voluntary attention is focused by purely internal decision processes (will), rather than instructions via external cues, we call this "willed attention." In prior work, we reported ERP and fMRI correlates of willed spatial attention in trial-by-trial cuing tasks. Here we further investigated the oscillatory mechanisms of willed attention by contrasting the event-related EEG spectrogram between instructional and choice cues. Two experiments were conducted at 2 different sites using the same visuospatial attention paradigm. Consistent between the 2 experiments, we found increases in frontal theta power (starting at ~500 ms post cue) for willed attention relative to instructed attention. This frontal theta increase was accompanied by increased frontal-parietal theta-band coherence and bidirectional Granger causality. Additionally, the onset of attention-related posterior alpha power lateralization was delayed in willed attention relative to instructed attention, and the amount of delay was related to the timing of frontal theta increase. These results, replicated across 2 experiments, suggest that theta oscillations are the neuronal signals indexing decision-making in the frontal cortex, and mediating reciprocal communications between the frontal executive and parietal attentional control regions during willed attention.

From eyes-closed to eyes-open: Role of cholinergic projections in EC-to-EO alpha reactivity revealed by combining EEG and MRI.

Alpha rhythm (8 to 12 Hz) observed in EEG over human posterior cortex is prominent during eyes-closed (EC) resting and attenuates during eyes-open (EO) resting. Research shows that the degree of EC-to-EO alpha blocking or alpha desynchronization, termed alpha reactivity here, is a neural marker of cognitive health. We tested the role of acetylcholine in EC-to-EO alpha reactivity by applying a multimodal neuroimaging approach to a cohort of young adults and a cohort of older adults. In the young cohort, simultaneous EEG-fMRI was recorded from twenty-one young adults during both EO and EC resting. In the older cohort, functional MRI was recorded from forty older adults during EO and EC resting, along with FLAIR and diffusion MRI. For a subset of twenty older adults, EEG was recorded during EO and EC resting in a separate session. In both young and older adults, functional connectivity between the basal nucleus of Meynert (BNM), the major source of cortical acetylcholine, and the visual cortex increased from EC to EO, and this connectivity increase was positively associated with alpha reactivity; namely, the stronger the BNM-visual cortex functional connectivity increase from EC to EO, the larger the EC-to-EO alpha desynchronization. In older adults, lesions of the fiber tracts linking BNM and visual cortex quantified by leukoaraiosis volume, associated with reduced alpha reactivity. These findings support a role of acetylcholine and particularly cholinergic pathways in mediating EC-to-EO alpha reactivity and suggest that impaired alpha reactivity could serve as a marker of the integrity of the cholinergic system.