Jesse J. Bengson

Top-down Modulation of Neural Activity in Anticipatory Visual Attention: Control Mechanisms Revealed by Simultaneous EEG-fMRI

In covert visual attention, frontoparietal attention control areas are thought to issue signals to selectively bias sensory neurons to facilitate behaviorally relevant information and suppress distraction. We investigated the relationship between activity in attention control areas and attention-related modulation of posterior alpha activity using simultaneous electroencephalography (EEG) and functional magnetic resonance imaging in humans during cued visual-spatial attention. Correlating single-trial EEG alpha power with blood-oxygen-level dependent (BOLD) activity, we found that BOLD in the intraparietal sulcus (IPS) and left middle frontal gyrus was inversely correlated with occipital alpha power. Importantly, in IPS, inverse correlations were stronger for alpha within the hemisphere contralateral to the attended hemifield, implicating the IPS in the enhancement of task-relevant sensory areas. Positive BOLD-alpha correlations were observed in sensorimotor cortices and the default mode network, suggesting a mechanism of active suppression over task-irrelevant areas. The magnitude of cue-induced alpha lateralization was positively correlated with BOLD in dorsal anterior cingulate cortex and dorsolateral prefrontal cortex, implicating a role of executive control in attention. These results show that IPS and frontal executive areas are the main sources of biasing influences on task-relevant visual cortex, whereas task-irrelevant default mode network and sensorimotor cortex are inhibited during visual attention.

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 semantic priming project.

Speeded naming and lexical decision data for 1,661 target words following related and unrelated primes were collected from 768 subjects across four different universities. These behavioral measures have been integrated with demographic information for each subject and descriptive characteristics for every item. Subjects also completed portions of the Woodcock–Johnson reading battery, three attentional control tasks, and a circadian rhythm measure. These data are available at a user-friendly Internet-based repository (http://spp.montana.edu). This Web site includes a search engine designed to generate lists of prime–target pairs with specific characteristics (e.g., length, frequency, associative strength, latent semantic similarity, priming effect in standardized and raw reaction times). We illustrate the types of questions that can be addressed via the Semantic Priming Project. These data represent the largest behavioral database on semantic priming and are available to researchers to aid in selecting stimuli, testing theories, and reducing potential confounds in their studies.

Spontaneous neural fluctuations predict decisions to attend

Ongoing variability in neural signaling is an intrinsic property of the brain. Often this variability is considered to be noise and ignored. However, an alternative view is that this variability is fundamental to perception and cognition and may be particularly important in decision-making. Here, we show that a momentary measure of occipital alpha-band power (8–13 Hz) predicts choices about where human participants will focus spatial attention on a trial-by-trial basis. This finding provides evidence for a mechanistic account of decision-making by demonstrating that ongoing neural activity biases voluntary decisions about where to attend within a given moment.

Normal aging selectively diminishes alpha lateralization in visual spatial attention

EEG studies of cue-induced visual alpha power (8-13 Hz) lateralization have been conducted on young adults without examining differences that may develop as a consequence of normal aging. Here, we examined age-related differences in spatial attention by comparing healthy older and younger adults. Our key finding is that cue-induced alpha power lateralization was observed in younger, but not older adults, even though both groups exhibited classic event-related potential signatures of spatial orienting. Specifically, both younger and older adults showed significant early directing-attention negativity (EDAN), anterior directing-attention negativity (ADAN), late directing-attention positivity (LDAP) and contingent negative variation (CNV). Furthermore, target-evoked sensory components were enhanced for attended relative to unattended targets in both younger and older groups. This pattern of results suggests that although older adults can successfully allocate spatial attention, they do so without the lateralization of alpha power that is commonly observed in younger adults. Taken together, our findings demonstrate that younger and older adults might engage different neural mechanisms for attentional orienting, and that alpha power lateralization during visual spatial attention is a phenomenon that diminishes during normal aging.

Individual working memory capacity is uniquely correlated with feature-based attention when combined with spatial attention

A growing literature suggests that working memory and attention are closely related constructs. Both involve the selection of task-relevant information, and both are characterized by capacity limits. Furthermore, studies using a variety of methodological approaches have demonstrated convergent working memory and attention-related processing at the individual, neural and behavioral level. Given the varieties of both constructs, the specific kinds of attention and WM must be considered. We find that individuals’ working memory capacity (WMC) uniquely interacts with feature-based attention when combined with spatial attention in a cuing paradigm (Posner, 1980). Our findings suggest a positive correlation between WM and feature-based attention only within the spotlight of spatial attention. This finding lends support to the controlled attention view of working memory by demonstrating that integrated feature-based expectancies are uniquely correlated with individual performance on a working memory task.

The neural correlates of volitional attention: A combined fMRI and ERP study

Studies of visual‐spatial attention typically use instructional cues to direct attention to a relevant location, but in everyday vision, attention is often focused volitionally, in the absence of external signals. Although investigations of cued attention comprise hundreds of behavioral and physiological studies, remarkably few studies of voluntary attention have addressed the challenging question of how spatial attention is initiated and controlled in the absence of external instructions, which we refer to as willed attention. To explore this question, we employed a trial‐by‐trial spatial attention task using electroencephalography and functional magnetic resonance imaging (fMRI). The fMRI results reveal a unique network of brain regions for willed attention that includes the anterior cingulate cortex, left middle frontal gyrus (MFG), and the left and right anterior insula (AI). We also observed two event‐related potentials (ERPs) associated with willed attention; one with a frontal distribution occurring 250–350 ms postdecision cue onset (EWAC: Early Willed Attention Component), and another occurring between 400 and 800 ms postdecision‐cue onset (WAC: Willed Attention Component). In addition, each ERP component uniquely correlated across subjects with different willed attention‐specific sites of BOLD activation. The EWAC was correlated with the willed attention‐specific left AI and left MFG activations and the later WAC was correlated only with left AI. These results offer a comprehensive and novel view of the electrophysiological and anatomical profile of willed attention and further illustrate the relationship between scalp‐recorded ERPs and the BOLD response. Hum Brain Mapp 36:2443–2454, 2015.

Age-related spatiotemporal reorganization during response inhibition.

As a key high-level cognitive function in human beings, response inhibition is crucial for adaptive behavior. Previous neuroimaging studies have shown that older individuals exhibit greater neural activation than younger individuals during response inhibition tasks. This finding has been interpreted within a neural compensation framework, in which additional neural resources are recruited in response to age-related cognitive decline. Although this interpretation has received empirical support, the precise event-related temporal course of this age-related compensatory neural response remains unexplored. In the present study, we conducted source analysis on inhibition-related ERP components (i.e., N2 and P3) that were recorded while healthy younger and older adults participated in a visual Go/NoGo task. We found that older adults showed increased source current densities of the N2 and P3 components than younger adults, which support previous hemodynamic findings. Further, such age-related differences in neural activation were successfully separated between the N2 and P3 periods by source localization analysis. Interestingly, the increased activations in older adults were primarily localized to the right precentral and postcentral gyri during the N2 period, which shifted to the right dorsolateral prefrontal cortex and the right inferior frontal gyrus during the P3 period. Taken together, our results clearly illustrate the spatiotemporal dynamics of age-related functional brain reorganization, and further specify the exact temporal course at the millisecond scale by which age-related compensatory neural responses occur during response inhibition.

The spotlight of attention illuminates failed feature‐based expectancies

A well-replicated finding is that visual stimuli presented at an attended location are afforded a processing benefit in the form of speeded reaction times and increased accuracy (Mangun, ; Posner,). This effect has been described using a spotlight metaphor, in which all stimuli within the focus of spatial attention receive facilitated processing, irrespective of other stimulus parameters. However, the spotlight metaphor has been brought into question by a series of combined expectancy studies that demonstrated that the behavioral benefits of spatial attention are contingent on secondary feature-based expectancies (Kingstone,). The present work used an event-related potential (ERP) approach to reveal that the early neural signature of the spotlight of spatial attention is not sensitive to the validity of secondary feature-based expectancies.

Effects of strategy on visual working memory capacity

Substantial evidence suggests that individual differences in estimates of working memory capacity reflect differences in how effectively people use their intrinsic storage capacity. This suggests that estimated capacity could be increased by instructions that encourage more effective encoding strategies. The present study tested this by giving different participants explicit strategy instructions in a change detection task. Compared to a condition in which participants were simply told to do their best, we found that estimated capacity was increased for participants who were instructed to remember the entire visual display, even at set sizes beyond their capacity. However, no increase in estimated capacity was found for a group that was told to focus on a subset of the items in supracapacity arrays. This finding confirms the hypothesis that encoding strategies may influence visual working memory performance, and it is contrary to the hypothesis that the optimal strategy is to filter out any items beyond the storage capacity.