Sustained selective attention in adolescence: Cognitive development and predictors of distractibility at school.

Despite much research into the development of attention in adolescence, mixed results and between-task differences have precluded clear conclusions regarding the relative early or late maturation of attention abilities. Moreover, although adolescents constantly face the need to pay attention at school, it remains unclear whether laboratory measures of attention can predict their ability to sustain attention focus during lessons. Therefore, here we devised a task that was sensitive to measure both sustained and selective attention and tested whether task measures could predict adolescents' levels of inattention during lessons. In total, 166 adolescents (aged 12-17 years) and 50 adults performed a sustained selective attention task, searching for letter targets while ignoring salient yet entirely irrelevant distractor faces, under different levels of perceptual load-an established determinant of attention in adults. Inattention levels during a just preceding classroom lesson were measured using a novel self-report classroom distractibility checklist. The results established that sustained attention (measured with response variability) continued to develop throughout adolescence across perceptual load levels. In contrast, there was an earlier maturation of the effect of perceptual load on selective attention; load modulation of distractor interference was larger in the early adolescence period compared with later periods. Both distractor interference and response variability were significant unique predictors of distractibility in the classroom, including when controlling for interest in the lesson and cognitive aptitude. Overall, the results demonstrate divergence of development of sustained and selective attention in adolescence and establish both as significant predictors of attention in the important educational setting of school lessons.

Attention and Capacity Limits in Perception: A Cellular Metabolism Account.

Limits on perceptual capacity result in various phenomena of inattentional blindness. Here we propose a neurophysiological account attributing these perceptual capacity limits directly to limits on cerebral cellular metabolism. We hypothesized that overall cerebral energy supply remains constant, regardless of overall mental processing demands; therefore, an attention mechanism is required to regulate limited cellular metabolism levels in line with attended task demands. Increased perceptual load in a task (imposing a greater demand on neural computations) should thus result in increased metabolism underlying attended processing, and reduced metabolism mediating unattended processing. We tested this prediction measuring oxidation states of cytochrome c oxidase (oxCCO), an intracellular marker of cellular metabolism. Broadband near-infrared spectroscopy was used to record oxCCO levels from human visual cortex while participants (both sexes) performed a rapid sequential visual search task under either high perceptual load (complex feature-conjunction search) or low load (feature pop-out search). A task-irrelevant, peripheral checkerboard was presented on a random half of trials. Our findings showed that oxCCO levels in visual cortex regions responsive to the attended-task stimuli were increased in high versus low perceptual load, whereas oxCCO levels related to unattended processing were significantly reduced. A negative temporal correlation of these load effects further supported our metabolism trade-off account. These results demonstrate an attentional compensation mechanism that regulates cellular metabolism levels according to processing demands. Moreover, they provide novel evidence for the widely held stipulation that overall cerebral metabolism levels remain constant regardless of mental task demand and establish a neurophysiological account for capacity limits in perception.SIGNIFICANCE STATEMENT We investigated whether capacity limits in perception can be explained by the effects of attention on the allocation of limited cellular metabolic energy for perceptual processing. We measured the oxidation state of cytochrome c oxidase, an intracellular measure of metabolism, in human visual cortex during task performance. The results showed increased levels of cellular metabolism associated with attended processing and reduced levels of metabolism underlying unattended processing when the task was more demanding. A temporal correlation between these effects supported an attention-directed metabolism trade-off. These findings support an account for inattentional blindness grounded in cellular biochemistry. They also provide novel evidence for the claim that cerebral processing is limited by a constant energy supply, which thus requires attentional regulation.

Auditory Figure-Ground Segregation Is Impaired by High Visual Load.

Figure-ground segregation is fundamental to listening in complex acoustic environments. An ongoing debate pertains to whether segregation requires attention or is "automatic" and preattentive. In this magnetoencephalography study, we tested a prediction derived from load theory of attention (e.g., Lavie, 1995) that segregation requires attention but can benefit from the automatic allocation of any "leftover" capacity under low load. Complex auditory scenes were modeled with stochastic figure-ground stimuli (Teki et al., 2013), which occasionally contained repeated frequency component "figures." Naive human participants (both sexes) passively listened to these signals while performing a visual attention task of either low or high load. While clear figure-related neural responses were observed under conditions of low load, high visual load substantially reduced the neural response to the figure in auditory cortex (planum temporale, Heschl's gyrus). We conclude that fundamental figure-ground segregation in hearing is not automatic but draws on resources that are shared across vision and audition.SIGNIFICANCE STATEMENT This work resolves a long-standing question of whether figure-ground segregation, a fundamental process of auditory scene analysis, requires attention or is underpinned by automatic, encapsulated computations. Task-irrelevant sounds were presented during performance of a visual search task. We revealed a clear magnetoencephalography neural signature of figure-ground segregation in conditions of low visual load, which was substantially reduced in conditions of high visual load. This demonstrates that, although attention does not need to be actively allocated to sound for auditory segregation to occur, segregation depends on shared computational resources across vision and hearing. The findings further highlight that visual load can impair the computational capacity of the auditory system, even when it does not simply dampen auditory responses as a whole.

Effects of visual short-term memory load and attentional demand on the contrast response function.

Visual short-term memory (VSTM) load leads to impaired perception during maintenance. Here, we fitted the contrast response function to psychometric orientation discrimination data while also varying attention demand during maintenance to investigate: (1) whether VSTM load effects on perception are mediated by a modulation of the contrast threshold, consistent with contrast gain accounts, or by the function asymptote (1 lapse rate), consistent with response gain accounts; and (2) whether the VSTM load effects on the contrast response function depend on the availability of attentional resources. We manipulated VSTM load via the number of items in the memory set in a color and location VSTM task and assessed the contrast response function for an orientation discrimination task during maintenance. Attention demand was varied through spatial cuing of the orientation stimulus. Higher VSTM load increased the estimated contrast threshold of the contrast response function without affecting the estimated asymptote, but only when the discrimination task demanded attention. When attentional demand was reduced (in the cued conditions), the VSTM load effects on the contrast threshold were eliminated. The results suggest that VSTM load reduces perceptual sensitivity by increasing contrast thresholds, suggestive of a contrast gain modulation mechanism, as long as the perceptual discrimination task demands attention. These findings support recent claims that attentional resources are shared between perception and VSTM maintenance processes.

Individual differences in parietal and frontal cortex structure predict dissociable capacities for perception and cognitive control.

Capacity limits in perception can lead to failures of awareness in situations that overload capacity, resulting in various phenomena of 'inattentional blindness'. In contrast, capacity limits in cognitive control over attention by working memory lead to increased processing of irrelevant distractors (reduced inattentional blindness). Here, using Voxel-Based Morphometry combined with Principal Components Analysis, we establish distinct brain-structural correlates of perceptual capacity, dissociable from those of cognitive control. Perceptual capacity was measured as the principal component accounting for variance across tasks of multiple object tracking, change blindness and rapid visual enumeration (i.e. 'subitizing'). Cognitive control capacity was measured as the principal component underlying performance of three different complex working memory span tasks (involving spatial, semantic and numerical domains). Volumetric differences in the right Inferior Parietal Lobule (IPL) were predictive of individual differences in perceptual capacity, while volumetric differences in left Middle Frontal Gyrus (MFG) (as well as lateral frontal and posterior cingulate cortex in a non-parametric analysis) were predictive of individual differences in cognitive control capacity. IPL remained a significant predictor of perceptual capacity when controlling for variance accounted for by cognitive control capacity and vice versa for the neural correlates of cognitive control. These results suggest that perceptual and cognitive control capacities represent dissociable and lasting, trait-like attributes which can be predicted from distinct signatures in regional grey matter.

Attention, mindwandering, and mood.

We tested the hypothesis that mindwandering and external distraction are both manifestations of a common state of reduced attention focus, and examined how both relate to reported level of happiness. We conducted real-time sampling of people's experience of mindwandering, irrelevant distraction (e.g. by music, phone, etc.), and happiness levels, in two studies with 524 people undertaking common daily-life activities. All irrelevant external distractions were positively correlated with mindwandering. Indeed mindwandering duration could be predicted from the reported duration of external distraction, when controlling for a range of background variables. An exploratory factor analysis of mindwandering and distraction reports suggested a single underlying construct. In addition, duration of irrelevant distraction by both mobile phones and mindwandering was significantly associated with reduced reported levels of happiness. The results are consistent with the hypothesis that that a state of reduced attention focus underlies both mindwandering and distractibility and clarify the link with happiness.

Inattentional Deafness: Visual Load Leads to Time-Specific Suppression of Auditory Evoked Responses.

Due to capacity limits on perception, conditions of high perceptual load lead to reduced processing of unattended stimuli (Lavie et al., 2014). Accumulating work demonstrates the effects of visual perceptual load on visual cortex responses, but the effects on auditory processing remain poorly understood. Here we establish the neural mechanisms underlying "inattentional deafness"--the failure to perceive auditory stimuli under high visual perceptual load. Participants performed a visual search task of low (target dissimilar to nontarget items) or high (target similar to nontarget items) load. On a random subset (50%) of trials, irrelevant tones were presented concurrently with the visual stimuli. Brain activity was recorded with magnetoencephalography, and time-locked responses to the visual search array and to the incidental presence of unattended tones were assessed. High, compared to low, perceptual load led to increased early visual evoked responses (within 100 ms from onset). This was accompanied by reduced early (∼ 100 ms from tone onset) auditory evoked activity in superior temporal sulcus and posterior middle temporal gyrus. A later suppression of the P3 "awareness" response to the tones was also observed under high load. A behavioral experiment revealed reduced tone detection sensitivity under high visual load, indicating that the reduction in neural responses was indeed associated with reduced awareness of the sounds. These findings support a neural account of shared audiovisual resources, which, when depleted under load, leads to failures of sensory perception and awareness. SIGNIFICANCE STATEMENT: The present work clarifies the neural underpinning of inattentional deafness under high visual load. The findings of near-simultaneous load effects on both visual and auditory evoked responses suggest shared audiovisual processing capacity. Temporary depletion of shared capacity in perceptually demanding visual tasks leads to a momentary reduction in sensory processing of auditory stimuli, resulting in inattentional deafness. The dynamic "push-pull" pattern of load effects on visual and auditory processing furthers our understanding of both the neural mechanisms of attention and of cross-modal effects across visual and auditory processing. These results also offer an explanation for many previous failures to find cross-modal effects in experiments where the visual load effects may not have coincided directly with auditory sensory processing.

Establishing the Attention-Distractibility Trait.

Failures to focus attention will affect any task engagement (e.g., at work, in the classroom, when driving). At the clinical end, distractibility is a diagnostic criterion of attention-deficit/hyperactivity disorder (ADHD). In this study, we examined whether the inability to maintain attentional focus varies in the overall population in the form of an attention-distractibility trait. To test this idea, we administered an ADHD diagnostic tool to a sample of healthy participants and assessed the relationship between ADHD symptoms and task distraction. ADHD symptom summary scores were significantly positively associated with distractor interference in letter-search and name-classification tasks (as measured by reaction time), as long as the distractors were irrelevant (cartoon images) rather than relevant (i.e., compatible or incompatible with target names). Higher perceptual load during a task eliminated distraction irrespective of ADHD score. These findings suggest the existence of an attention-distractibility trait that confers vulnerability to irrelevant distraction, which can be remedied by increasing the level of perceptual load during the task.

Alleviating memory impairment through distraction.

Distraction typically has a negative impact on memory for recent events and patients with existing memory impairment are particularly vulnerable to distractor interference. In contrast, here we establish a beneficial effect for distractor presentation in humans for both patients with memory impairment due to bilateral hippocampal lesions and healthy adults with low memory performance. Recognition memory for images of place scenes, which had to be memorized for short delay periods was significantly improved with the presentation of a distractor face during the delay. Magnetoencephalography recordings of neural oscillations in the theta frequency range obtained in healthy adults suggest that this memory improvement results from the interruption of rehearsal by the distractor. Our results highlight circumstances where active memory rehearsal may paradoxically increase memory impairments and distraction alleviates these memory deficits in patients with hippocampal injury and healthy adults.

High perceptual load leads to both reduced gain and broader orientation tuning.

Due to its limited capacity, visual perception depends on the allocation of attention. The resultant phenomena of inattentional blindness, accompanied by reduced sensory visual cortex response to unattended stimuli in conditions of high perceptual load in the attended task, are now well established (Lavie, 2005; Lavie, 2010, for reviews). However, the underlying mechanisms for these effects remain to be elucidated. Specifically, is reduced perceptual processing under high perceptual load a result of reduced sensory signal gain, broader tuning, or both? We examined this question with psychophysical measures of orientation tuning under different levels of perceptual load in the task performed. Our results show that increased perceptual load leads to both reduced sensory signal and broadening of tuning. These results clarify the effects of attention on elementary visual perception and suggest that high perceptual load is critical for attentional effects on sensory tuning.

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.

Establishing gaze markers of perceptual load during multi-target visual search.

Highly-automated technologies are increasingly incorporated into existing systems, for instance in advanced car models. Although highly automated modes permit non-driving activities (e.g. internet browsing), drivers are expected to reassume control upon a 'take over' signal from the automation. To assess a person's readiness for takeover, non-invasive eye tracking can indicate their attentive state based on properties of their gaze. Perceptual load is a well-established determinant of attention and perception, however, the effects of perceptual load on a person's ability to respond to a takeover signal and the related gaze indicators are not yet known. Here we examined how load-induced attentional state affects detection of a takeover-signal proxy, as well as the gaze properties that change with attentional state, in an ongoing task with no overt behaviour beyond eye movements (responding by lingering the gaze). Participants performed a multi-target visual search of either low perceptual load (shape targets) or high perceptual load (targets were two separate conjunctions of colour and shape), while also detecting occasional auditory tones (the proxy takeover signal). Across two experiments, we found that high perceptual load was associated with poorer search performance, slower detection of cross-modal stimuli, and longer fixation durations, while saccade amplitude did not consistently change with load. Using machine learning, we were able to predict the load condition from fixation duration alone. These results suggest monitoring fixation duration may be useful in the design of systems to track users' attentional states and predict impaired user responses to stimuli outside of the focus of attention.

Visual short-term memory load reduces retinotopic cortex response to contrast.

Load Theory of attention suggests that high perceptual load in a task leads to reduced sensory visual cortex response to task-unrelated stimuli resulting in "load-induced blindness" [e.g., Lavie, N. Attention, distraction and cognitive control under load. Current Directions in Psychological Science, 19, 143-148, 2010; Lavie, N. Distracted and confused?: Selective attention under load. Trends in Cognitive Sciences, 9, 75-82, 2005]. Consideration of the findings that visual STM (VSTM) involves sensory recruitment [e.g., Pasternak, T., & Greenlee, M. Working memory in primate sensory systems. Nature Reviews Neuroscience, 6, 97-107, 2005] within Load Theory led us to a new hypothesis regarding the effects of VSTM load on visual processing. If VSTM load draws on sensory visual capacity, then similar to perceptual load, high VSTM load should also reduce visual cortex response to incoming stimuli leading to a failure to detect them. We tested this hypothesis with fMRI and behavioral measures of visual detection sensitivity. Participants detected the presence of a contrast increment during the maintenance delay in a VSTM task requiring maintenance of color and position. Increased VSTM load (manipulated by increased set size) led to reduced retinotopic visual cortex (V1-V3) responses to contrast as well as reduced detection sensitivity, as we predicted. Additional visual detection experiments established a clear tradeoff between the amount of information maintained in VSTM and detection sensitivity, while ruling out alternative accounts for the effects of VSTM load in terms of differential spatial allocation strategies or task difficulty. These findings extend Load Theory to demonstrate a new form of competitive interactions between early visual cortex processing and visual representations held in memory under load and provide a novel line of support for the sensory recruitment hypothesis of VSTM.

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.

Hippocampus-dependent and -independent theta-networks of active maintenance.

Recent studies in humans and animals raise the possibility that actively maintaining a detailed memory of a scene within working memory may require the hippocampus, a brain structure better known for its role in long-term memory. We show that the hippocampus is behaviorally and functionally critical for configural-relational (CR) maintenance by orchestrating the synchrony of occipital and temporal brain regions in the theta-frequency range. Using magnetoencephalography in healthy adults and patients with bilateral hippocampal sclerosis, we distinguish this hippocampus-dependent theta-network from one that is independent of the hippocampus and used for non-CR scene maintenance. This non-CR theta-network involved frontal and parietal brain regions. We also show that the functional and topographical dissociation between these two networks cannot be accounted for by perceptual difficulty or the amount of information to be maintained ("load"). Also, we confirm in healthy adults that active maintenance of the CR arrangement of objects within a scene is impaired by task-interference during the delay in a manner akin to working-memory maintenance processes. Together, these findings demand reconsideration of the classical functional-anatomical distinctions between long- and short-term memory.

Alpha oscillations reflect suppression of distractors with increased perceptual load.

Attention serves an essential role in cognition and behavior allowing us to focus on behaviorally-relevant objects while ignoring distraction. Perceptual load theory states that attentional resources are allocated according to the requirements of the task, i.e., its 'load'. The theory predicts that the resources left to process irrelevant, possibly distracting stimuli, are reduced when the perceptual load is high. However, it remains unclear how this allocation of attentional resources specifically relates to neural excitability and suppression mechanisms. In this magnetoencephalography (MEG) study, we show that brain oscillations in the alpha band (8-13 Hz) implemented the suppression of distracting objects when the perceptual load was high. In parallel, high load increased the neuronal excitability for target objects, as reflected by rapid invisible frequency tagging. We suggest that the allocation of resources in tasks with high perceptual load is implemented by a gain increase for targets, complemented by distractor suppression reflected by alpha-band oscillations closing the 'gate' for interference.

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.

Perceptual load and enumeration: Distractor interference depends on subitizing capacity.

Attention is limited, both in processing capacity (leading to phenomena of "inattentional blindness") and in the capacity for selective focus (leading to distraction). Load theory (e.g., Lavie, 1995) accounts for both limitations by proposing that perceptual processing has limited capacity but proceeds automatically and in parallel on all stimuli within capacity. Here we tested these claims by applying load theory to the phenomenon of "subitizing": the parallel detection and individuation of a limited number of items, established in enumeration research. We predicted that distractor interference will be found within but not beyond a person's subitizing capacity (measured as the transition from parallel to serial slope). Participants reported the number of target shapes from brief displays while ignoring irrelevant cartoon-image distractors. As predicted, distractor cost on enumeration performance was found within subitizing capacity and eliminated in larger set sizes. Moreover, individual differences results demonstrated that distractor effects depended on an individual's capacity (i.e., their serial-to-parallel transition point), rather than on set size per se. These results provide new evidence for the load theory hypotheses that perceptual processing is automatic and parallel within its limited capacity, while extending it to account for selective attention during enumeration. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Faces are not always special for attention: Effects of response-relevance and identity.

Research over the past 25 years indicates that stimulus processing is diminished when attention is engaged in a perceptually demanding task of high 'perceptual load'. These results have generalized across a variety of stimulus categories, but a controversy evolved over the question of whether perception of distractor faces (or other categories of perceptual expertise) can proceed irrespective of the level of perceptual load in the attended task. Here we identify task-relevance, and in particular identity-relevance, as a potentially important factor in explaining prior inconsistencies. In four experiments, we tested whether perceptual load in an attended letter or word task modulates the processing of famous face distractors, while varying their task-relevance. Distractor interference effects on task RTs was reduced by perceptual load not only when the faces were entirely task-irrelevant, but also when the face gender was task relevant, within a name gender classification response-competition task, using famous female or male distractor faces. However, when the identity associated with the famous faces was primed by the task using their names, as in prior demonstrations that face distractors are immune to the effects of perceptual load, we were able to replicate these prior findings. Our findings demonstrate a role for identity-priming by the relevant task in determining attentional capture by faces under high perceptual load. Our results also highlight the importance of considering even relatively subtle forms of task-relevance in selective attention research.

Attentional load modulates responses of human primary visual cortex to invisible stimuli.

Visual neuroscience has long sought to determine the extent to which stimulus-evoked activity in visual cortex depends on attention and awareness. Some influential theories of consciousness maintain that the allocation of attention is restricted to conscious representations [1, 2]. However, in the load theory of attention [3], competition between task-relevant and task-irrelevant stimuli for limited-capacity attention does not depend on conscious perception of the irrelevant stimuli. The critical test is whether the level of attentional load in a relevant task would determine unconscious neural processing of invisible stimuli. Human participants were scanned with high-field fMRI while they performed a foveal task of low or high attentional load. Irrelevant, invisible monocular stimuli were simultaneously presented peripherally and were continuously suppressed by a flashing mask in the other eye [4]. Attentional load in the foveal task strongly modulated retinotopic activity evoked in primary visual cortex (V1) by the invisible stimuli. Contrary to traditional views [1, 2, 5, 6], we found that availability of attentional capacity determines neural representations related to unconscious processing of continuously suppressed stimuli in human primary visual cortex. Spillover of attention to cortical representations of invisible stimuli (under low load) cannot be a sufficient condition for their awareness.