Attentional inhibition of visual processing in human striate and extrastriate cortex

Allocating attention to a spatial location in the visual field is associated with an increase in the cortical response evoked by a stimulus at that location, compared to when the same stimulus is unattended. We used event-related functional magnetic resonance imaging to investigate attentional modulation of the cortical response to a stimulus probe at an attended location and to multiple probes at unattended locations. A localizer task and retinotopic mapping were used to precisely identify the cortical representations of each probe within striate (V1) and extrastriate cortex (V2, VP, V3, V4v, and V3A). The magnitude and polarity of attentional modulation were assessed through analysis of event-related activity time-locked to shifts in spatial attention. Attentional facilitation at the attended location was observed in striate and extrastriate cortex, corroborating earlier findings. Attentional inhibition of visual stimuli near the attended location was observed in striate cortex, and attentional inhibition of more distant stimuli occurred in both striate and extrastriate cortex. These findings indicate that visual attention operates both through facilitation of visual processing at the attended location and through inhibition of unattended stimulus representations in striate and extrastriate cortex.     

fMRI reveals that involuntary visual deviance processing is resource limited

Previous studies suggest that involuntary auditory attention evoked by unattended auditory stimuli is not influenced by the primary focus of attention. However, prior studies from our laboratory have found that processing of unattended auditory deviant tones in the auditory and frontal regions is modulated by top-down attentional demands and resource availability. Whether processing of unattended visual deviant stimuli is altered by the availability of attentional resources has not been established. The goal of the current study was to examine the automaticity of these activations, their modulation by attentional capacity, and the neuroanatomical distribution of any attentional effects upon visual deviance detection. We designed an event-related functional magnetic resonance imaging (fMRI) study during which subjects performed a continuous perceptual-motor-visual tracking task whose difficulty was modulated by changing the control dynamics of a joystick. Changes in the anatomical localization, spatial distribution, and intensity of the blood oxygenation level-dependent (BOLD) response associated with unattended infrequent visual changes were examined during low- and high-difficulty tracking conditions of the primary visual task. Results revealed that the unattended deviants elicited BOLD activation in the visual, fusiform, and parietal regions. In these regions, the intensity and extent of the activation evoked by the deviants decreased as a function of the demands of the primary visual task. These findings suggest that processing of unattended visual deviant stimuli is restricted by the attentional demands of a primary task, as previously demonstrated for unattended auditory deviant tones.     

Selective influences of cross-modal spatial-cues on preattentive auditory processing: a whole-head magnetoencephalography study

The processing streams of the various sensory modalities are known to interact within the central nervous system. These interactions differ depending on the level of stimulus representation and attention. The current study focused on cross-sensory influences on stimulus change detection during unattended auditory processing. We employed an oddball paradigm to assess cortical processing using whole-head magnetoencephalography (MEG) in 20 volunteers. While subjects performed distraction tasks of varying difficulties, auditory duration deviants were applied randomly to the left or the right ear preceded (200-400 ms) by oculomotor, static visual, or flow field co-stimulation at either side. Mismatch fields were recorded over both hemispheres. Changes in gaze direction and static visual stimuli elicited the most reliable enhancement of deviance detection at the same side (most prominent at the right auditory cortex). Under both conditions, the lateralized unattended and unpredictive pre-cues acted analogously to shifts in selective attention, but were not reduced by attentional load. Thus, the early cognitive representation of sounds seems to reflect automatic cross-modal interference. Preattentive multisensory integration may provide the neuronal basis for orienting reactions to objects in space and thus for voluntary control of selective attention.     

Cortical dynamics of selective attention to somatosensory events

Recent studies have shown evidence of somatosensory deficits in individuals with attentional difficulties yet relatively little is known about the role of attention in the processing of somatosensory input. Neuromagnetic imaging studies have shown that rhythmic oscillations within the human somatosensory cortex are strongly modulated by somatosensory stimulation and may reflect the normal processing of such stimuli. However, few studies have examined how attention influences these cortical oscillations. We examined attentional effects on human somatosensory oscillations during median nerve stimulation by conducting time–frequency analyses of neuromagnetic recordings in healthy adults. We found that selective attention modulated somatosensory oscillations in the alpha, beta, and gamma bands that were both phase-locked and non-phase-locked to the stimulus. In the primary somatosensory cortex (SI), directing the subject's attention toward the somatosensory stimulus resulted in increased gamma band power (30–55 Hz) that was phase-locked to stimulus onset. Directed attention also produced an initial suppression (desynchrony) followed by enhancement (synchrony) of beta band power (13–25 Hz) that was not phase-locked to the stimulus. In the secondary somatosensory cortex (SII), directing attention towards the stimulus increased phase-locked alpha (7–9 Hz) power approximately 30 ms after onset of phase-locked gamma in SI, followed by a non-phase-locked increase in alpha power. We suggest that earlier phase-locked oscillatory power may reflect the relay of input from SI to SII, whereas later non-phase-locked rhythms reflect stimulus-induced oscillations that are modulated by selective attention and may thus reflect enhanced processing of the stimulus underlying the perception of somatosensory events.     

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.     

Steady-state responses in MEG demonstrate information integration within but not across the auditory and visual senses

To form a unified percept of our environment, the human brain integrates information within and across the senses. This MEG study investigated interactions within and between sensory modalities using a frequency analysis of steady-state responses that are elicited time-locked to periodically modulated stimuli. Critically, in the frequency domain, interactions between sensory signals are indexed by crossmodulation terms (i.e. the sums and differences of the fundamental frequencies). The 3 × 2 factorial design, manipulated (1) modality: auditory, visual or audiovisual (2) steady-state modulation: the auditory and visual signals were modulated only in one sensory feature (e.g. visual gratings modulated in luminance at 6 Hz) or in two features (e.g. tones modulated in frequency at 40 Hz & amplitude at 0.2 Hz). This design enabled us to investigate crossmodulation frequencies that are elicited when two stimulus features are modulated concurrently (i) in one sensory modality or (ii) in auditory and visual modalities. In support of within-modality integration, we reliably identified crossmodulation frequencies when two stimulus features in one sensory modality were modulated at different frequencies. In contrast, no crossmodulation frequencies were identified when information needed to be combined from auditory and visual modalities. The absence of audiovisual crossmodulation frequencies suggests that the previously reported audiovisual interactions in primary sensory areas may mediate low level spatiotemporal coincidence detection that is prominent for stimulus transients but less relevant for sustained SSR responses. In conclusion, our results indicate that information in SSRs is integrated over multiple time scales within but not across sensory modalities at the primary cortical level.     

A crossmodal crossover: opposite effects of visual and auditory perceptual load on steady-state evoked potentials to irrelevant visual stimuli

Mechanisms of attention are required to prioritise goal-relevant sensory events under conditions of stimulus competition. According to the perceptual load model of attention, the extent to which task-irrelevant inputs are processed is determined by the relative demands of discriminating the target: the more perceptually demanding the target task, the less unattended stimuli will be processed. Although much evidence supports the perceptual load model for competing stimuli within a single sensory modality, the effects of perceptual load in one modality on distractor processing in another is less clear. Here we used steady-state evoked potentials (SSEPs) to measure neural responses to irrelevant visual checkerboard stimuli while participants performed either a visual or auditory task that varied in perceptual load. Consistent with perceptual load theory, increasing visual task load suppressed SSEPs to the ignored visual checkerboards. In contrast, increasing auditory task load enhanced SSEPs to the ignored visual checkerboards. This enhanced neural response to irrelevant visual stimuli under auditory load suggests that exhausting capacity within one modality selectively compromises inhibitory processes required for filtering stimuli in another.     

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.     

Attention-dependent changes of activation and connectivity in dichotic listening

Functional studies of auditory spatial attention generally report enhanced neural responses in auditory cortical regions. However, activity in regions of the spatial attentional network as described in the visual modality is not consistently observed. Data analysis limitations due to oppositely lateralized activity depending on the side of attentional orientation and heterogeneity of paradigms makes it hard to untangle the possible causes of these various activation patterns. In the present article we present a PET study of auditory spatial attention in which we manipulated orientation of attention, attentional load, and difficulty of the task by means of the dichotic listening paradigm. Moreover, we designed a systematic, voxel-specific, method in order to deal with oppositely lateralized activity. The results show that when listeners are involved in auditory spatial attention tasks an interacting network of frontal, temporal, and parietal regions is activated. Selective orientation toward one side mostly yields activity and connectivity modulations in the hemisphere contralateral to the attended side while in divided attention activity is mostly bilateral. Taken together, our observations are consistent with the idea of a multimodal large-scale attentional network.     

fMRI during natural sleep as a method to study brain function during early childhood

Many techniques to study early functional brain development lack the whole-brain spatial resolution that is available with fMRI. We utilized a relatively novel method in which fMRI data were collected from children during natural sleep. Stimulus-evoked responses to auditory and visual stimuli as well as stimulus-independent functional networks were examined in typically developing 2-4-year-old children. Reliable fMRI data were collected from 13 children during presentation of auditory stimuli (tones, vocal sounds, and nonvocal sounds) in a block design. Twelve children were presented with visual flashing lights at 2.5 Hz. When analyses combined all three types of auditory stimulus conditions as compared to rest, activation included bilateral superior temporal gyri/sulci (STG/S) and right cerebellum. Direct comparisons between conditions revealed significantly greater responses to nonvocal sounds and tones than to vocal sounds in a number of brain regions including superior temporal gyrus/sulcus, medial frontal cortex and right lateral cerebellum. The response to visual stimuli was localized to occipital cortex. Furthermore, stimulus-independent functional connectivity MRI analyses (fcMRI) revealed functional connectivity between STG and other temporal regions (including contralateral STG) and medial and lateral prefrontal regions. Functional connectivity with an occipital seed was localized to occipital and parietal cortex. In sum, 2-4 year olds showed a differential fMRI response both between stimulus modalities and between stimuli in the auditory modality. Furthermore, superior temporal regions showed functional connectivity with numerous higher-order regions during sleep. We conclude that the use of sleep fMRI may be a valuable tool for examining functional brain organization in young children.     

Stimuli of varying spatial scale induce gamma activity with distinct temporal characteristics in human visual cortex

Gamma activity to stationary grating stimuli was studied non-invasively using MEG recordings in humans. Using a spatial filtering technique, we localized gamma activity to primary visual cortex. We tested the hypothesis that spatial frequency properties of visual stimuli may be related to the temporal frequency characteristics of the associated cortical responses. We devised a method to assess temporal frequency differences between stimulus-related responses that typically exhibit complex spectral shapes. We applied this methodology to either single-trial (induced) or time-averaged (evoked) responses in four frequency ranges (0-40, 20-60, 40-80 and 60-100 Hz) and two time windows (either the entire duration of stimulus presentation or the first second following stimulus onset). Our results suggest that stimuli of varying spatial frequency induce responses that exhibit significantly different temporal frequency characteristics. These effects were particularly accentuated for induced responses in the classical gamma frequency band (20-60 Hz) analyzed over the entire duration of stimulus presentation. Strikingly, examining the first second of the responses following stimulus onset resulted in significant loss in stimulus specificity, suggesting that late signal components contain functionally relevant information. These findings advocate a functional role of gamma activity in sensory representation. We suggest that stimulus specific frequency characteristics of MEG signals can be mapped to processes of neuronal synchronization within the framework of coupled dynamical systems.     

The temporal frequency tuning of human visual cortex investigated using synthetic aperture magnetometry

Using synthetic aperture magnetometry (SAM) analyses of magnetoencephalographic (MEG) data, we investigated the variation in cortical response magnitude and frequency as a function of stimulus temporal frequency. In two separate experiments, a reversing checkerboard stimulus was used in the right or left lower visual field at frequencies from 0 to 21 Hz. Average temporal frequency tuning curves were constructed for regions-of-interest located within medial visual cortex and V5/MT. In medial visual cortex, it was found that both the frequency and magnitude of the steady-state response varied as a function of the stimulus frequency, with multiple harmonics of the stimulus frequency being found in the response. The maximum fundamental response was found at a stimulus frequency of 8 Hz, whilst the maximum broadband response occurred at 4 Hz. In contrast, the magnitude and frequency content of the evoked onset response showed no dependency on stimulus frequency. Whilst medial visual cortex showed a power increase during stimulation, extra-striate areas such as V5/MT exhibited a bilateral event-related desynchronisation (ERD). The frequency content of this ERD did not depend on the stimulus frequency but was a broadband power reduction across the 5-20 Hz frequency range. The magnitude of this ERD within V5/MT was strongly low-pass tuned for stimulus frequency, and showed only a moderate preference for stimuli in the contralateral visual field.     

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.     

Cortical source estimates of gamma band amplitude and phase are different in schizophrenia

Reductions in gamma band phase synchrony and evoked power have been reported in schizophrenic subjects in response to auditory stimuli. These results have been observed in the EEG at one or two electrode sites. We wished to extend these results using magnetic field data to estimate the responses at the neural generators themselves in each hemisphere. Whole head magnetoencephalographic (MEG) recordings were used to estimate the phase and amplitude behavior of sources in primary auditory cortex in both hemispheres of schizophrenic and comparison subjects. Both ipsi- and contralateral cases were evaluated using a driving (40 Hz modulated 1 kHz carrier) and a non-driving (1 kHz tone) stimulus. We used source space projection (SSP) to collapse the magnetic field data into estimates of the time course of source strengths in individual trials. Complex wavelet based time–frequency decomposition was used to compute inter-trial phase locking factor (PLF), and mean evoked and induced amplitude for each cortical generator. Schizophrenic subjects showed reduced SSP PLF and evoked source strength for contralateral generators responding to the driving stimulus in both hemispheres. For the pure tone stimulus, only the left hemisphere PLF's in the transient window were reduced. In contrast, subjects with schizophrenia exhibited higher induced 40 Hz power to both stimulus types, consistent with the reduced PLF findings. The method of SSP combined with wavelet based complex demodulation produces a significant improvement in signal-to-noise ratio, and directly estimates the activity of the cortical generators responsible for gamma band auditory MEG evoked fields. Schizophrenic subjects exhibit significant impairment of generation and phase locking of this activity in auditory cortex, suggesting an impairment of GABA-ergic inhibitory interneuronal modulation of pyramidal cell activity.     

Differential patterns of multisensory interactions in core and belt areas of human auditory cortex

The auditory cortex is anatomically segregated into a central core and a peripheral belt region, which exhibit differences in preference to bandpassed noise and in temporal patterns of response to acoustic stimuli. While it has been shown that visual stimuli can modify response magnitude in auditory cortex, little is known about differential patterns of multisensory interactions in core and belt. Here, we used functional magnetic resonance imaging and examined the influence of a short visual stimulus presented prior to acoustic stimulation on the spatial pattern of blood oxygen level-dependent signal response in auditory cortex. Consistent with crossmodal inhibition, the light produced a suppression of signal response in a cortical region corresponding to the core. In the surrounding areas corresponding to the belt regions, however, we found an inverse modulation with an increasing signal in centrifugal direction. Our data suggest that crossmodal effects are differentially modulated according to the hierarchical core-belt organization of auditory cortex.     

Sustained spatial attention to vibration is mediated in primary somatosensory cortex

Focusing attention to a specific body location has been shown to improve processing of events presented at this body location. One important debate concerns the stage in the somatosensory pathway at which the neural response is modulated when one attends to a tactile stimulus. Previous studies focused on components of the somatosensory evoked potential to transient stimuli, and demonstrated an early cortical attentional modulation. The neural basis of sustained spatial stimulus processing with continuous stimulation remains, however, largely unexplored. A way to approach this topic is to present vibrating stimuli with different frequencies for several seconds simultaneously to different body locations while subjects have to attend to the one or the other location. The amplitude of the somatosensory steady-state evoked potential (SSSEP) elicited by these vibrating stimuli increases with attention. On the basis of 128 electrode recordings, we investigated the topographical distribution and the underlying cortical sources by means of a VARETA approach of this attentional amplitude modulation of the SSSEP. Sustained spatial attention was found to be mediated in primary somatosensory cortex with no differences in SSSEP amplitude topographies between attended and unattended body locations. These result patterns were seen as evidence for a low-level sensory gain control mechanism in tactile spatial attention.     

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.     

It's only in your head: expectancy of aversive auditory stimulation modulates stimulus-induced auditory cortical alpha desynchronization

Increasing evidence underlines the functional importance of non-phase-locked cortical oscillatory rhythms. Among the different oscillations, alpha (8-12 Hz) has been shown to be modulated by anticipation or attention, suggesting a top-down influence. However, most studies to date have been conducted in the visual modality and the extent to which this notion also applies to the auditory cortex is unclear. It is furthermore often difficult to dissociate bottom-up from top-down contributions in cases of different stimuli (e.g., standards vs. deviants) or stimuli that are preceded by different cues. This study addresses these issues by investigating neuronal responses associated with intrinsically fluctuating perceptions of an invariant sound. Sixteen participants performed a pseudo-frequency-discrimination task in which a "high-pitch" tone was followed by an aversive noise, while the "low-pitch" tone was followed by silence. The participants had to decide which tone was presented even though the stimulus was actually kept constant while pseudo-randomized feedback was given. EEG data show that auditory cortical alpha power decreased by 20% in "high-pitch" trials relative to trials in which a "low pitch" was perceived. This study shows that expectancy of aversive feedback modulates perception of sounds and these fluctuating perceptions become manifest in modulations of sound-related alpha desynchronizations. Our findings extend recent evidence in the visual and somatosensory domain that alpha oscillations represent the excitatory/inhibitory balance of sensory cortical cell assemblies, which can be tuned in a top-down manner.     

Prestimulus oscillations predict visual perception performance between and within subjects

In the present study, the electrophysiological correlates of perceiving shortly presented visual stimuli are examined. In particular, we investigated the differences in the prestimulus EEG between subjects who were able to discriminate between four shortly presented stimuli (Perceivers) and subjects who were not (Non-Perceivers). Additionally, we investigated the differences between the subjects perceived and unperceived trials. The results show that Perceivers exhibited lower prestimulus alpha power than Non-Perceivers. Analysis of the prestimulus EEG between perceived and unperceived trials revealed that the perception of a stimulus is related to low phase coupling in the alpha frequency range (8-12 Hz) and high phase coupling in the beta and gamma frequency range (20-45 Hz). Single trial analyses showed that perception performance can be predicted by phase coupling in the alpha, beta and gamma frequency range. The findings indicate that synchronous oscillations in the alpha frequency band inhibit the perception of shortly presented stimuli whereas synchrony in higher frequency ranges (>20 Hz) enhances visual perception. We conclude that alpha, beta and gamma oscillations indicate the attentional state of a subject and thus are able to predict perception performance on a single trial basis.