Todd A. Kelley

Attentional modulation of repetition attenuation is anatomically dissociable for scenes and faces

Repeating a stimulus generally leads to a decreased response in neural activity compared to that for novel items. This neural attenuation provides a marker for stimulus-specific perceptual encoding and memory that can be detected using functional magnetic resonance imaging (fMRI). Although previously assumed to occur automatically whenever a stimulus is repeated, recent studies have begun to show that the repetition attenuation effect is task-specific and modulated by attention. Here, we demonstrate that attention is crucial for obtaining neural attenuation even after extensive stimulus repetitions. Furthermore, the effect of attention on attenuation is anatomically dissociable for stimuli that have relatively segregated neural representations in high-level perceptual cortex. To manipulate attention, we used overlapping scene and face images, and asked subjects to attend to either category. In a scene-sensitive cortical region known as the parahippocampal place area (PPA), significant attenuation in the fMRI BOLD signal was observed for the attended repeated scenes (relative to attended novel scenes), while no attenuation was observed for ignored repeated scenes or attended repeated faces against their respective novel image baselines. Conversely, in the face-sensitive region known as the fusiform face area (FFA), significant attenuation was observed for attended repeated faces, but not for ignored repeated faces or attended repeated scenes. An additional control experiment ruled out alternative explanations based on global signal level reductions due to inattention. Thus, attention actively governed when neuronal activity was attenuated to repeated perceptual input, and such attenuation was specific to the cortical regions that actively represent the attended category of stimuli.

Working Memory Load Modulates Distractor Competition in Primary Visual Cortex

When stimuli compete for sensory processing and response selection, coherent goal-guided behavior requires cognitive control so that task-relevant “targets” rather than irrelevant distractors are selected. It has been shown that reduced cognitive control under high working memory load increases distractor competition for selection. It remains unknown, though, whether cognitive control by working memory has an effect on the earliest levels of sensory processing in primary visual cortex. The present study addressed this question by having subjects perform a selective attention task involving classification of meaningful target objects while also ignoring congruent and incongruent distractor images. The level of cognitive control over distractor competition was varied through a concurrent working memory task of either low (1 digit) or high (6 digits) load. Functional magnetic resonance imaging revealed greater distractor competition effects not only on behavior but also on the sensory correlates in primary visual cortex (areas V1–V2) in conditions of high (vs. low) working memory load. In addition, high working memory load resulted in increased congruency-related functional connectivity between anterior cingulate cortex and V1. These results are the first to establish the neural correlates of distractor competition effects in primary visual cortex and the critical role of working memory in their cognitive control.

Learning to attend: effects of practice on information selection.

Though practice can lead to improved performance in many domains, it is currently unknown how practice affects the deployment of selective attention to filter distracting information. We conducted a series of experiments to address this issue by examining how performance on a task changed after repeated exposure to distractors. Distraction initially slowed response time during task performance, an effect that diminished with repeated exposure to the distractors. When the distractors were consistent in appearance, the practice effect developed quickly but was stimulus-specific. When the distractors were more variable in appearance, the practice effect developed slowly but transferred more readily to other conditions. These data indicate that practice with overcoming distraction leads to improvements in information filtering mechanisms that generalize beyond the training regimen when variable distractor stimuli are experienced.

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.

Neural Correlates of Learning to Attend

Recent work has shown that training can improve attentional focus. Little is known, however, about how training in attention and multitasking affects the brain. We used functional magnetic resonance imaging (fMRI) to measure changes in cortical responses to distracting stimuli during training on a visual categorization task. Training led to a reduction in behavioral distraction effects, and these improvements in performance generalized to untrained conditions. Although large regions of early visual and posterior parietal cortices responded to the presence of distractors, these regions did not exhibit significant changes in their response following training. In contrast, middle frontal gyrus did exhibit decreased distractor-related responses with practice, showing the same trend as behavior for previously observed distractor locations. However, the neural response in this region diverged from behavior for novel distractor locations, showing greater activity. We conclude that training did not change the robustness of the initial sensory response, but led to increased efficiency in late-stage filtering in the trained conditions.

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.

Enhanced visual perception with occipital transcranial magnetic stimulation

Transcranial magnetic stimulation (TMS) over the occipital pole can produce an illusory percept of a light flash (or ‘phosphene’), suggesting an excitatory effect. Whereas previous reported effects produced by single‐pulse occipital pole TMS are typically disruptive, here we report the first demonstration of a location‐specific facilitatory effect on visual perception in humans. Observers performed a spatial cueing orientation discrimination task. An orientation target was presented in one of two peripheral placeholders. A single pulse below the phosphene threshold applied to the occipital pole 150 or 200 ms before stimulus onset was found to facilitate target discrimination in the contralateral compared with the ipsilateral visual field. At the 150‐ms time window contralateral TMS also amplified cueing effects, increasing both facilitation effects for valid cues and interference effects for invalid cues. These results are the first to show location‐specific enhanced visual perception with single‐pulse occipital pole stimulation prior to stimulus presentation, suggesting that occipital stimulation can enhance the excitability of visual cortex to subsequent perception.

The impact of distractor congruency on stimulus processing in retinotopic visual cortex

The brain is frequently confronted with sensory information that elicits conflicting response choices. While much research has addressed the top down control mechanisms associated with detection and resolution of response competition, the effects of response competition on sensory processing in the primary visual cortex remain unclear. To address this question we modified a typical ‘flanker task’ (Eriksen and Eriksen, 1974) so that the effects of response competition on human early retinotopic visual cortex could be assessed. Healthy human participants were scanned using fMRI while making a speeded choice response that classified a target object image into one of two categories (e.g. fruits, animals). An irrelevant distractor image that was either congruent (same image as target), incongruent (image from opposite category as target), or neutral (image from task-irrelevant category, e.g. household items) was also present on each trial, but in a different quadrant of the visual field relative to the target. Retinotopic V1 areas responding to the target stimuli showed increased response to targets in the presence of response-incongruent (compared to response-neutral) distractors. A negative correlation with behavioral response competition effects indicated that an increased primary visual cortical response to targets in the incongruent (vs. neutral) trials is associated with a reduced response competition effect on behavior. These results suggest a novel conflict resolution mechanism in the primary visual cortex.

Deciding where to attend: Large-scale network mechanisms underlying attention and intention revealed by graph-theoretic analysis

&NA; The neural mechanisms by which intentions are transformed into actions remain poorly understood. We investigated the network mechanisms underlying spontaneous voluntary decisions about where to focus visual‐spatial attention (willed attention). Graph‐theoretic analysis of two independent datasets revealed that regions activated during willed attention form a set of functionally‐distinct networks corresponding to the frontoparietal network, the cingulo‐opercular network, and the dorsal attention network. Contrasting willed attention with instructed attention (where attention is directed by external cues), we observed that the dorsal anterior cingulate cortex was allied with the dorsal attention network in instructed attention, but shifted connectivity during willed attention to interact with the cingulo‐opercular network, which then mediated communications between the frontoparietal network and the dorsal attention network. Behaviorally, greater connectivity in network hubs, including the dorsolateral prefrontal cortex, the dorsal anterior cingulate cortex, and the inferior parietal lobule, was associated with faster reaction times. These results, shown to be consistent across the two independent datasets, uncover the dynamic organization of functionally‐distinct networks engaged to support intentional acts. HighlightsWilled attention is supported by three functionally distinct networks.The dACC reorganized its connectivity according to task demand.The cingulo‐opercular network mediated network‐level communication.Network hubs included the dACC, rDLPFC, and rIPL.

Attention induced neural response trade-off in retinotopic cortex under load

The effects of perceptual load on visual cortex response to distractors are well established and various phenomena of ‘inattentional blindness’ associated with elimination of visual cortex response to unattended distractors, have been documented in tasks of high load. Here we tested an account for these effects in terms of a load-induced trade-off between target and distractor processing in retinotopic visual cortex. Participants were scanned using fMRI while performing a visual-search task and ignoring distractor checkerboards in the periphery. Retinotopic responses to target and distractors were assessed as a function of search load (comparing search set-sizes two, three and five). We found that increased load not only increased activity in frontoparietal network, but also had opposite effects on retinotopic responses to target and distractors. Target-related signals in areas V2–V3 linearly increased, while distractor response linearly decreased, with increased load. Critically, the slopes were equivalent for both load functions, thus demonstrating resource trade-off. Load effects were also found in displays with the same item number in the distractor hemisphere across different set sizes, thus ruling out local intrahemispheric interactions as the cause. Our findings provide new evidence for load theory proposals of attention resource sharing between target and distractor leading to inattentional blindness.