An fMRI study of reduced perceptual load-dependent modulation of task-irrelevant activity in adults with autism spectrum conditions

Recent studies on selective attention have demonstrated that the perceptual load of a task determines the processing stage at which irrelevant sensory stimuli are filtered out. Although individuals with autism spectrum conditions (ASC) have been repeatedly reported to display several kinds of abnormal behavior related to attention deficits, the neural mechanisms underlying these deficits have not been well investigated within the framework of the load dependency of selective attention. The present study used functional magnetic resonance imaging (fMRI) to examine the brain responses of adults with high-functioning ASC to irrelevant visual distractors while performing a visual target detection task under high or low perceptual load. We observed that the increased perceptual load activated regions of the fronto-parietal attention network of controls and ASC comparably. On the other hand, the visual cortex activity evoked by visual distractors was less modulated by the increased perceptual load in ASC than in controls. Simple regression analyses showed that the degree of the modulation was significantly correlated with the severity of the autistic symptoms. We also observed reduced load-dependent modulation of the functional connectivity between the intraparietal and visual regions in the ASC group. These results revealed neural correlates for abnormal perceptual load-dependent engagement of visual attention in ASC, which may underlie aspects of cognitive and behavioral characteristics of these disorders.     

Human brain activity associated with audiovisual perception and attention

Coherent perception of objects in our environment often requires perceptual integration of auditory and visual information. Recent behavioral data suggest that audiovisual integration depends on attention. The current study investigated the neural basis of audiovisual integration using 3-Tesla functional magnetic resonance imaging (fMRI) in 12 healthy volunteers during attention to auditory or visual features, or audiovisual feature combinations of abstract stimuli (simultaneous harmonic sounds and colored circles). Audiovisual attention was found to modulate activity in the same frontal, temporal, parietal and occipital cortical regions as auditory and visual attention. In addition, attention to audiovisual feature combinations produced stronger activity in the superior temporal cortices than attention to only auditory or visual features. These modality-specific areas might be involved in attention-dependent perceptual binding of synchronous auditory and visual events into coherent audiovisual objects. Furthermore, the modality-specific temporal auditory and occipital visual cortical areas showed attention-related modulations during both auditory and visual attention tasks. This result supports the proposal that attention to stimuli in one modality can spread to encompass synchronously presented stimuli in another modality.     

Impact of brain networks involved in vigilance on processing irrelevant visual motion

The ability to sustain attention over prolonged periods of time is called vigilance. Vigilance is a fundamental component of attention which impacts on performance in many situations. We here investigate whether similar neural mechanisms are responsible for vigilant attention over long and short durations of time and whether neural activity in brain regions sensitive to vigilant attention is related to processing irrelevant information. Brain activity was measured by means of functional magnetic resonance imaging (fMRI) in a 32 min visual vigilance task with varying inter-target intervals and irrelevant peripheral motion stimuli. Changes in neural activity were analysed as a function of time on task to capture long-term aspects of vigilance and as a function of time between target stimuli to capture short-term aspects of vigilance. Several brain regions including the inferior frontal, posterior parietal, superior and middle temporal cortices and the anterior insular showed decreases in neural activity as a function of time on task. In contrast, increasing inter-target intervals resulted in increased neural activity in a widespread network of regions involving lateral and medial frontal areas, temporal areas, cuneus and precuneus, inferior occipital cortex (right), posterior insular cortices, the thalamus, nucleus accumbens and basal forebrain. A partial least square analysis revealed that neural activity in this latter network covaried with neural activity related to processing irrelevant motion stimuli. Our results provide neural evidence that two separate mechanisms are responsible for sustaining attention over long and short durations. We show that only brain areas involved in sustaining attention over short durations of time are related to processing irrelevant stimuli and suggest that these areas can be segregated into two functionally different networks, one possibly involved in motivation, the other in arousal.     

Processing of angry voices is modulated by visual load

Visual perceptual load has been shown to modulate brain activation to emotional facial expressions. However, it is unknown whether cross-modal effects of visual perceptual load on brain activation to threat-related auditory stimuli also exist. The current fMRI study investigated brain responses to angry and neutral voices while subjects had to solve an easy or a demanding visual task. Although the easy visual condition was associated with increased activation in the right superior temporal region to angry vs. neutral prosody, this effect was absent during the demanding task. Thus, our results show that cross-modal perceptual load modulates the activation to emotional voices in the auditory cortex and that high visual load prevents the increased processing of emotional prosody.     

The effect of visuospatial attentional load on the processing of irrelevant acoustic distractors

This work investigated the role of cognitive control functions in selective attention when task-relevant and -irrelevant stimuli come from different sensory modalities. We parametrically manipulated the load of an attentive tracking task and investigated its effect on irrelevant acoustic change-related processing. While subjects were performing the visual attentive tracking task, event-related potentials (ERPs) were recorded for frequent standard tones and rare deviant tones presented as auditory distractors. The deviant tones elicited two change-related ERP components: the mismatch negativity (MMN) and the P3a. The amplitude of the MMN, which indexes the early detection of irregular changes, increased with increasing attentional load, whereas the subsequent P3a component, which indicates the involuntary orienting of attention to deviants, was significant only in the lowest load condition. These findings suggest that active exclusion of the early detection process of irrelevant acoustic changes depends on available resources of cognitive control, whereas the late involuntary orienting of attention to deviants can be passively suppressed by high demand on central attentional resources. The present study thus reveals opposing visual attentional load effects at different temporal and functional stages in the rejection of deviant auditory distractors and provides a new perspective on the resolution of the long-standing early versus late attention selection debate.     

Emotion modulates the effects of endogenous attention on retinotopic visual processing

A fundamental challenge for organisms is how to focus on perceptual information relevant to current goals while remaining able to respond to goal-irrelevant stimuli that signal potential threat. Here, we studied how visual threat signals influence the effects of goal-directed spatial attention on the retinotopic distribution of processing resources in early visual cortex. We used a combined blocked and event-related functional magnetic resonance imaging paradigm with target displays comprising diagonal pairs of intact and scrambled faces presented simultaneously in the four visual field quadrants. Faces were male or female and had fearful or neutral emotional expressions. Participants attended covertly to a pair of two diagonally opposite stimuli and performed a gender-discrimination task on the attended intact face. In contrast to the fusiform face area, where attention and fearful emotional expression had additive effects, neural responses to attended and unattended fearful faces were indistinguishable in early retinotopic visual areas: When attended, fearful face expression did not further enhance responses, whereas when unattended, fearful expression increased responses to the level of attended face stimuli. Remarkably, the presence of fearful stimuli augmented the enhancing effect of attention on retinotopic responses to neutral faces in remote visual field locations. We conclude that this redistribution of neural activity in retinotopic visual cortex may serve the purpose of allocating processing resources to task-irrelevant threat-signaling stimuli while at the same time increasing resources for task-relevant stimuli as required for the maintenance of goal-directed behavior.     

Estimating the influence of attention on population codes in human visual cortex using voxel-based tuning functions

In order to form stable perceptual representations, populations of sensory neurons must pool their output to overcome physiological noise; selective attention is then required to ensure that behaviorally relevant stimuli dominate these 'population codes' to gain access to awareness. However, the role that attention plays in shaping population response profiles has received little direct investigation, in part because most traditional neurophysiological methods cannot simultaneously assess changes in activity across large populations of sensory neurons. Based on single-unit recording studies, current theories hold that attending to a relevant feature sharpens the population response profile and improves the signal-to-noise ratio of the resulting perceptual representation. Here, we test this hypothesis using fMRI and an analysis approach that is able to estimate the influence of feature-based attentional modulations on population response profiles. We first derive orientation tuning functions for single voxels in human primary visual cortex, and then use these tuning functions to sort voxels according to their orientation preference. We then show that selective attention systematically biases population response profiles so that behaviorally relevant stimuli are represented in the visual system at the expense of behaviorally irrelevant stimuli. Collectively, the present results (1) provide a new approach for precisely characterizing feature-selective responses in human sensory cortices and (2) reveal how behavioral goals can shape population response profiles to support the formation of coherent perceptual representations.     

Attentional and linguistic interactions in speech perception

The role of attention in speech comprehension is not well understood. We used fMRI to study the neural correlates of auditory word, pseudoword, and nonspeech (spectrally rotated speech) perception during a bimodal (auditory, visual) selective attention task. In three conditions, Attend Auditory (ignore visual), Ignore Auditory (attend visual), and Visual (no auditory stimulation), 28 subjects performed a one-back matching task in the assigned attended modality. The visual task, attending to rapidly presented Japanese characters, was designed to be highly demanding in order to prevent attention to the simultaneously presented auditory stimuli. Regardless of stimulus type, attention to the auditory channel enhanced activation by the auditory stimuli (Attend Auditory>Ignore Auditory) in bilateral posterior superior temporal regions and left inferior frontal cortex. Across attentional conditions, there were main effects of speech processing (word+pseudoword>rotated speech) in left orbitofrontal cortex and several posterior right hemisphere regions, though these areas also showed strong interactions with attention (larger speech effects in the Attend Auditory than in the Ignore Auditory condition) and no significant speech effects in the Ignore Auditory condition. Several other regions, including the postcentral gyri, left supramarginal gyrus, and temporal lobes bilaterally, showed similar interactions due to the presence of speech effects only in the Attend Auditory condition. Main effects of lexicality (word>pseudoword) were isolated to a small region of the left lateral prefrontal cortex. Examination of this region showed significant word>pseudoword activation only in the Attend Auditory condition. Several other brain regions, including left ventromedial frontal lobe, left dorsal prefrontal cortex, and left middle temporal gyrus, showed Attention x Lexicality interactions due to the presence of lexical activation only in the Attend Auditory condition. These results support a model in which neutral speech presented in an unattended sensory channel undergoes relatively little processing beyond the early perceptual level. Specifically, processing of phonetic and lexical-semantic information appears to be very limited in such circumstances, consistent with prior behavioral studies.     

Changing channels: an fMRI study of aging and cross-modal attention shifts

Age-related deficits in visual selective attention suggest that the efficiency of inhibitory processes is particularly affected by aging. To investigate whether processing inefficiencies observed in visual attention are similar in auditory attention and when shifting attention across modalities, we conducted an fMRI study with healthy young and older adults using a task that required sustained auditory and visual selective attention and cross-modal attention shifts. Older adults in this study performed as well as the younger adults, but showed age-related differences in BOLD responses. The most striking of these differences were bilateral frontal and parietal regions of significantly increased activation in older adults during both focused and shifting attention. Our data suggest that this increased activation did not reflect new recruitment, but reliance on brain regions typically used by younger adults when task demands are greater. Older adults' activation patterns suggested that even during focused attention conditions they were "shifting" attention to stimuli in the unattended modality. Increased activation during processing of both task-relevant and task-irrelevant information implies age-related loss of processing selectivity. These patterns may reflect both task-specific compensatory neural recruitment and degradation of sensory inhibition.     

Cross-modal processing in auditory and visual working memory

This study aimed to further explore processing of auditory and visual stimuli in working memory. Smith and Jonides (1997) [Smith, E.E., Jonides, J., 1997. Working memory: A view from neuroimaging. Cogn. Psychol. 33, 5-42] described a modified working memory model in which visual input is automatically transformed into a phonological code. To study this process, auditory and the corresponding visual stimuli were presented in a variant of the 2-back task which involved changes from the auditory to the visual modality and vice versa. Brain activation patterns underlying visual and auditory processing as well as transformation mechanisms were analyzed. Results yielded a significant activation in the left primary auditory cortex associated with transformation of visual into auditory information which reflects the matching and recoding of a stored item and its modality. This finding yields empirical evidence for a transformation of visual input into a phonological code, with the auditory cortex as the neural correlate of the recoding process in working memory.     

Reduced visual processing capacity in sleep deprived persons

Multiple experiments have found sleep deprivation to lower task-related parietal and extrastriate visual activation, suggesting a reduction of visual processing capacity in this state. The perceptual load theory of attention (Lavie, 1995) predicts that our capacity to process unattended distractors will be reduced by increasing perceptual difficulty of task-relevant stimuli. Here, we evaluated the effects of sleep deprivation and perceptual load on visual processing capacity by measuring neural repetition-suppression to unattended scenes while healthy volunteers attended to faces embedded in face-scene pictures. Perceptual load did not affect repetition suppression after a normal night of sleep. Sleep deprivation reduced repetition suppression in the parahippocampal place area (PPA) in the high but not low perceptual load condition. Additionally, the extent to which task-related fusiform face area (FFA) activation was reduced after sleep deprivation correlated with behavioral performance and lowered repetition suppression in the PPA. The findings concerning correct responses indicate that a portion of stimulus related activation following a normal night of sleep contributes to potentially useful visual processing capacity that is attenuated following sleep deprivation. Finally, when unattended stimuli are not highly intrusive, sleep deprivation does not appear to increase distractibility.     

Interaction between stimulus intensity and perceptual load in the attentional control of pain

The interaction between intensity of nociceptive stimuli and cognitive load in a concomitant task is still a challenging and complex topic. Here, we investigated the interaction between top-down factors (i.e., perceptual load), induced by a visual task, and bottom-up factors (i.e., intensity of nociceptive stimuli that implicitly modifies saliency of input). Using a new experimental paradigm, in which perceptual load is varied while laser heat stimuli of different intensities are processed; we show a significant interaction between intensity of nociceptive stimuli and perceptual load on both pain ratings and task performance. High perceptual load specifically reduced intensity ratings of high intensity stimuli. However, under this condition, task performance was impaired, regardless of interindividual differences in motivation and pain catastrophizing. Thus, we showed that pain ratings can be reduced by increasing the load of attentional resources at the perceptual level of a non–pain-related task. Nevertheless, the disruptive effect of highly intensive nociceptive stimuli on the performance of the perceptual task was evident only under high load.     

The neural basis of visual dominance in the context of audio-visual object processing

Visual dominance refers to the observation that in bimodal environments vision often has an advantage over other senses in human. Therefore, a better memory performance for visual compared to, e.g., auditory material is assumed. However, the reason for this preferential processing and the relation to the memory formation is largely unknown. In this fMRI experiment, we manipulated cross-modal competition and attention, two factors that both modulate bimodal stimulus processing and can affect memory formation. Pictures and sounds of objects were presented simultaneously in two levels of recognisability, thus manipulating the amount of cross-modal competition. Attention was manipulated via task instruction and directed either to the visual or the auditory modality. The factorial design allowed a direct comparison of the effects between both modalities. The resulting memory performance showed that visual dominance was limited to a distinct task setting. Visual was superior to auditory object memory only when allocating attention towards the competing modality. During encoding, cross-modal competition and attention towards the opponent domain reduced fMRI signals in both neural systems, but cross-modal competition was more pronounced in the auditory system and only in auditory cortex this competition was further modulated by attention. Furthermore, neural activity reduction in auditory cortex during encoding was closely related to the behavioural auditory memory impairment. These results indicate that visual dominance emerges from a less pronounced vulnerability of the visual system against competition from the auditory domain.     

Modality effects in verbal working memory: differential prefrontal and parietal responses to auditory and visual stimuli

The neural bases of verbal (nonspatial) working memory (VWM) have been primarily examined using visual stimuli. Few studies have investigated the neural bases of VWM using auditory stimuli, and fewer have explored modality differences in VWM. In this study, we used functional magnetic resonance imaging (fMRI) to examine similarities and differences between visual VWM (vis-VWM) and auditory VWM (aud-VWM) utilizing identical stimuli and a within-subjects design. Performance levels were similar in the two modalities and there was extensive overlap of activation bilaterally in the dorsolateral and ventrolateral prefrontal cortex (DLPFC and VLPFC), intraparietal sulcus, supramarginal gyrus and the basal ganglia. However, a direct statistical comparison revealed significant modality differences: the left posterior parietal cortex, primarily along the intraparietal sulcus, showed greater responses during vis-VWM whereas the left dorsolateral prefrontal cortex showed greater responses during aud-VWM. No such differences were observed in the right hemisphere. Other modality differences in VWM were also observed, but they were associated with relative decreases in activation. In particular, we detected bilateral suppression of the superior and middle temporal (auditory) cortex during vis-VWM, and of the occipital (visual) cortex during aud-VWM, thus suggesting that cross-modal inhibitory processes may help to provide preferential access to high-order heteromodal association areas. Taken together, our findings suggest that although similar prefrontal and parietal regions are involved in aud-VWM and vis-VWM, there are important modality differences in the way neural signals are generated, processed and routed during VWM.     

When and where perceptual load interacts with voluntary visuospatial attention: an event-related potential and dipole modeling study

Perceptual load is recognized to affect visual selective attention, but at an unknown spatiotemporal locus in the brain. To examine this issue, event-related potentials (ERPs) were recorded while participants performed an orientation discrimination task, under conditions of low or high perceptual load. Participants were required to respond to targets (10% of trials) presented in the attended visual field while ignoring all stimuli in the unattended visual field. The interaction between voluntary attention and perceptual load was significant for the posterior N1 component (190 ms) but not for the earlier C1 (84 ms) or P1 (100 ms) components. This load by attention interaction for N1 was localized to the temporoparietal-occipital (TPO) gyrus by dipole modeling analysis. Dipole modeling also showed that a reversed attentional effect in the C1 time range was due to ERP overlap from the subsequent attention-sensitive P1 component. Results suggest that perceptual load affects voluntary visuospatial attention at an early (but not the earliest) processing stage and that the TPO gyrus mediates target selection at the discrimination stage.     

Attention and Vigilance in Children with Down Syndrome

Background Down syndrome (DS) has been the focus of much cognitive and developmental research; however, there is a gap in knowledge regarding sustained attention, particularly across different sensory domains. This research examined the hypothesis that children with DS would demonstrate superior visual rather than auditory performance on a sustained attention task and that this modality difference would not be seen in children with non‐specific intellectual disability (NSID). Materials and Methods Eleven children with DS and 16 children with NSID were compared on two versions of the sustained attention to response test (SART), varying only in presentation modality (visual or auditory). Errors of commission (failure to withhold response to target) and errors of omission (failure to respond to non‐target distractors) were recorded. Results Significant group differences were found in the visual modality and mental age was also found to effect error rates in the visual condition. No effect of group or mental age was observed in the auditory SART. Conclusions Results suggest that, for individuals with DS, presentation of education material in a visual medium may facilitate sustained attention and thus learning. Further research using tools such as the SART to explore modality differences in sustained attention and additional cognitive domains is recommended.     

State-dependent attention modulation of human primary visual cortex: a high density ERP study

Converging electrophysiological and brain-imaging results show that sensory processing in V1 can be modulated by attention. In this study, we tested the prediction that this early filtering effect depends on the current affective state of the participant. We recorded visual evoked potentials (VEPs) to visual peripheral distractors while participants performed a demanding task at fixation, whose perceptual load was manipulated in a parametric fashion. Crucially, levels of negative affect were either increased or decreased independently of changes in perceptual load. Concurrent psychophysiological measurements and self-report scales confirmed that changes in emotional state were effective. In the control condition, ERP results showed that the C1 component generated in response to the exact same peripheral distractors systematically varied in amplitude with the amount of perceptual load imposed at fixation, being larger when perceptual load decreased. However, this early modulatory effect in V1 was disrupted when participants transiently experienced increased state anxiety, resulting in a decreased C1 amplitude even though task load at fixation remained low. These results suggest that early bottom-up processing in V1 is not only influenced by the amount of attention resources available, but also by the current internal state of the participant.     

Differences in early sensory-perceptual processing in synesthesia: a visual evoked potential study

Synesthesia is a condition where stimulation of a single sensory modality or processing stream elicits an idiosyncratic, yet reliable perception in one or more other modalities or streams. Various models have been proposed to explain synesthesia, which have in common aberrant cross-activation of one cortical area by another. This has been observed directly in cases of linguistic-color synesthesia as cross-activation of the 'color area', V4, by stimulation of the grapheme area. The underlying neural substrates that mediate cross-activations in synesthesia are not well understood, however. In addition, the overall integrity of the visual system has never been assessed and it is not known whether wider differences in sensory-perceptual processing are associated with the condition. To assess whether fundamental differences in perceptual processing exist in synesthesia, we utilised high-density 128-channel electroencephalography (EEG) to measure sensory-perceptual processing using stimuli that differentially bias activation of the magnocellular and parvocellular pathways of the visual system. High and low spatial frequency gratings and luminance-contrast squares were presented to 15 synesthetes and 15 controls. We report, for the first time, early sensory-perceptual differences in synesthetes relative to non-synesthete controls in response to simple stimuli that do not elicit synesthetic color experiences. The differences are manifested in the early sensory components of the visual evoked potential (VEP) to stimuli that bias both magnocellular and parvocellular responses, but are opposite in direction, suggesting a differential effect on these two pathways. We discuss our results with reference to widespread connectivity differences as a broader phenotype of synesthesia.     

Reciprocal modulation of neuromagnetic induced gamma activity by attention in the human visual and auditory cortex

For attentional control of behavior, the brain permanently resolves a competition between the impressions supplied by different senses. Here, using a dual-modality temporal order detection task, we studied attentional modulation of oscillatory neuromagnetic activity in the human cerebral cortex. On each trial, after simultaneous exposure to visual and auditory noise, subjects were presented with an asynchronous pair of a visual and an auditory stimulus. Either of the two stimuli could occur first equally often, their order was not cued. Subjects had to determine the leading stimulus in a pair and attentively monitor it to respond upon its offset. With the attended visual or auditory stimuli, spectral power analysis revealed marked enhancements of induced gamma activity within 250 ms post-stimulus onset over the modality-specific cortices (occipital at 64 Hz, right temporal at 53 Hz). When unattended, however, the stimuli led to a significantly decreased (beneath baseline) gamma response in these cortical regions. The gamma decreases occurred at lower frequencies ( approximately 30 Hz) than did the gamma increases. An increase in the gamma power and frequency for the attended modality and their decrease for the unattended modality suggest that attentional regulation of multisensory processing involves reciprocal changes in synchronization of respective cortical networks. We assume that the gamma decrease reflects an active suppression of the task-irrelevant sensory input. This suppression occurs at lower frequencies, suggesting an involvement of larger scale cell assemblies.     

Older adults, unlike younger adults, do not modulate alpha power to suppress irrelevant information

This study examines the neural mechanisms through which younger and older adults ignore irrelevant information, a process that is necessary to effectively encode new memories. Some age-related memory deficits have been linked to a diminished ability to dynamically gate sensory input, resulting in problems inhibiting the processing of distracting stimuli. Whereas oscillatory power in the alpha band (8-12Hz) over visual cortical areas is thought to dynamically gate sensory input in younger adults, it is not known whether older adults use the same mechanism to gate out sensory input. Here we identified a task in which both older and younger adults could suppress the processing of irrelevant sensory stimuli, allowing us to use electroencephalography (EEG) to explore the neural activity associated with suppression of visual processing. As expected, we found that the younger adults' suppression of visual processing was correlated with robust modulation of alpha oscillatory power. However, older adults did not modulate alpha power to suppress processing of visual information. These results demonstrate that suppression of alpha power is not necessary to inhibit the processing of distracting stimuli in older adults, suggesting the existence of alternative strategies for suppressing irrelevant, potentially distracting information.