Cortical mechanisms of feature-based attentional control

A network of fronto-parietal cortical areas is known to be involved in the control of visual attention, but the representational scope and specific function of these areas remains unclear. Recent neuroimaging evidence has revealed the existence of both transient (attention-shift) and sustained (attention-maintenance) mechanisms of space-based and object-based attentional control. Here we investigate the neural mechanisms of feature-based attentional control in human cortex using rapid event-related functional magnetic resonance imaging (fMRI). Subjects viewed an aperture containing moving dots in which dot color and direction of motion changed once per second. At any given moment, observers attended to either motion or color. Two of six motion directions and two of six colors embedded in the stimulus stream cued subjects either to shift attention from the currently attended to the unattended feature or to maintain attention on the currently attended feature. Attentional modulation of the blood oxygenation level dependent (BOLD) fMRI signal was observed in early visual areas that are selective for motion and color. More importantly, both transient and sustained BOLD activity patterns were observed in different fronto-parietal cortical areas during shifts of attention. We suggest these differing temporal profiles reflect complementary roles in the control of attention to perceptual features.     

Spatio-temporal analysis of feature-based attention

The cortical mechanisms of feature-selective attention to color and motion cues were studied in humans using combined electrophysiological, magnetoencephalographic, and hemodynamic (functional magnetic resonance imaging) measures of brain activity. Subjects viewed a display of random dots that periodically either changed color or moved coherently. When attention was directed to the color change it elicited enhanced neural activity in visual area V4v, previously shown to be specialized for processing color information. In contrast, when dot movement was attended it produced enhanced activity in the motion-specialized area human MT. Parallel recordings of event-related electrophysiological and magnetoencephalographic responses indicated that the attention-related facilitation of neural activity in these specialized cortical areas occurred rapidly, beginning as early as 90-120 ms after stimulus onset. We conclude that selection of an entire feature dimension (motion or color) boosts neural activity in its specialized cortical module much more rapidly than does selection of one feature value from another (e.g., one color from another), as reported in previous electrophysiological studies. By combining methods with high spatial and temporal resolution it is possible to analyze the precise time course of feature-selective processing in specialized cortical areas.     

Parametric merging of MEG and fMRI reveals spatiotemporal differences in cortical processing of spoken words and environmental sounds in background noise

There is an increasing interest to integrate electrophysiological and hemodynamic measures for characterizing spatial and temporal aspects of cortical processing. However, an informative combination of responses that have markedly different sensitivities to the underlying neural activity is not straightforward, especially in complex cognitive tasks. Here, we used parametric stimulus manipulation in magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) recordings on the same subjects, to study effects of noise on processing of spoken words and environmental sounds. The added noise influenced MEG response strengths in the bilateral supratemporal auditory cortex, at different times for the different stimulus types. Specifically for spoken words, the effect of noise on the electrophysiological response was remarkably nonlinear. Therefore, we used the single-subject MEG responses to construct parametrization for fMRI data analysis and obtained notably higher sensitivity than with conventional stimulus-based parametrization. fMRI results showed that partly different temporal areas were involved in noise-sensitive processing of words and environmental sounds. These results indicate that cortical processing of sounds in background noise is stimulus specific in both timing and location and provide a new functionally meaningful platform for combining information obtained with electrophysiological and hemodynamic measures of brain function.     

The effects of stimulus modality and frequency of stimulus presentation on cross-modal distraction

Selective attention produces enhanced activity (attention-related modulations [ARMs]) in cortical regions corresponding to the attended modality and suppressed activity in cortical regions corresponding to the ignored modality. However, effects of behavioral context (e.g., temporal vs. spatial tasks) and basic stimulus properties (i.e., stimulus frequency) on ARMs are not fully understood. The current study used functional magnetic resonance imaging to investigate selectively attending and responding to either a visual or auditory metronome in the presence of asynchronous cross-modal distractors of 3 different frequencies (0.5, 1, and 2 Hz). Attending to auditory information while ignoring visual distractors was generally more efficient (i.e., required coordination of a smaller network) and less effortful (i.e., decreased interference and presence of ARMs) than attending to visual information while ignoring auditory distractors. However, these effects were modulated by stimulus frequency, as attempting to ignore auditory information resulted in the obligatory recruitment of auditory cortical areas during infrequent (0.5 Hz) stimulation. Robust ARMs were observed in both visual and auditory cortical areas at higher frequencies (2 Hz), indicating that participants effectively allocated attention to more rapidly presented targets. In summary, results provide neuroanatomical correlates for the dominance of the auditory modality in behavioral contexts that are highly dependent on temporal processing.     

The neural substrates of biological motion perception: an fMRI study

We used fMRI to identify the brain areas related to the perception of biological motion (4 T EPI; whole brain). In experiment 1, 10 subjects viewed biological motion (a human figure jumping up and down, composed of 21 dots), alternating with a control stimulus created by applying autoregressive models to the biological motion stimulus (such that the dots' speeds and amplitudes were preserved whereas their linking structure was not). The lengths of the stimulus bouts varied, and therefore the transitions between biological motion and control stimuli were unpredictable. Subjects had to indicate with a button press when each transition occurred. In a related biological motion task, subjects detected short (1 s) disturbances within these displays. We also examined the neural substrates of motion and shape perception, as well as motor imagery, to determine whether or not the cortical regions involved in these processes are also recruited during biological motion perception. Subjects viewed linear motion displays alternating with static dots and a series of common objects alternating with band-limited white noise patterns. Subjects also generated imagery of their own arm movements alternating with visual imagery of common objects. Biological motion specific BOLD signal was found within regions of the lingual gyrus at the cuneus border, showing little overlap with object recognition, linear motion or motion imagery areas. The lingual gyrus activation was replicated in a second experiment that also mapped retinotopic visual areas in three subjects. The results suggest that a region of the lingual gyrus within VP is involved in higher-order processing of motion information.     

An fMRI version of the Farnsworth-Munsell 100-Hue test reveals multiple color-selective areas in human ventral occipitotemporal cortex.

Studies of patients with cerebral achromatopsia have suggested that ventral occipitotemporal cortex is important for color perception. We created a functional magnetic resonance imaging (fMRI) version of a clinical test commonly used to assess achromatopsia, the Farnsworth-Munsell 100-Hue test. The test required normal subjects to use color information in the visual stimulus to perform a color sequencing task. A modification of the test requiring ordering by luminance was used as a control task. Subjects were also imaged as they passively viewed colored stimuli. A limited number of areas responded more to chromatic than achromatic stimulation, including primary visual cortex. Most color-selective activity was concentrated in ventral occipitotemporal cortex. Several areas in ventral cortex were identified. The most posterior, located in posterior fusiform gyrus, corresponded to the area activated by passive viewing of colored stimuli. More anterior and medial color-selective areas were located in the collateral sulcus and fusiform gyrus. These more anterior areas were not identified in previous imaging studies which used passive viewing of colored stimuli, and were most active in our study when visual color information was behaviorally relevant, suggesting that attention influences activity in color-selective areas. The fMRI version of the Farnsworth-Munsell test may be useful in the study of achromatopsia.     

On the variability of the McGurk effect: audiovisual integration depends on prestimulus brain states

The McGurk effect demonstrates the influence of visual cues on auditory perception. Mismatching information from both sensory modalities can fuse to a novel percept that matches neither the auditory nor the visual stimulus. This illusion is reported in 60-80% of trials. We were interested in the impact of ongoing brain oscillations-indexed by fluctuating local excitability and interareal synchronization-on upcoming perception of identical stimuli. The perception of the McGurk effect is preceded by high beta activity in parietal, frontal, and temporal areas. Beta activity is pronounced in the left superior temporal gyrus (lSTG), which is considered as a site of multimodal integration. This area is functionally (de)coupled to distributed frontal and temporal regions in illusion trials. The disposition to fuse multisensory information is enhanced as the lSTG is more strongly coupled to frontoparietal regions. Illusory perception is accompanied by a decrease in poststimulus theta-band activity in the cuneus, precuneus, and left superior frontal gyrus. Event-related activity in the left middle temporal gyrus is pronounced during illusory perception. Thus, the McGurk effect depends on fluctuating brain states suggesting that functional connectedness of left STS at a prestimulus stage is crucial for an audiovisual percept.     

Neural sources of focused attention in visual search

Previous studies of visual search in humans using event-related potentials (ERPs) have revealed an ERP component called 'N2pc' (180-280 ms) that reflects the focusing of attention onto potential target items in the search array. The present study was designed to localize the neuroanatomical sources of this component by means of magnetoencephalographic (MEG) recordings, which provide greater spatial precision than ERP recordings. MEG recordings were obtained with an array of 148 magnetometers from six normal adult subjects, one of whom was tested in multiple sessions so that both single-subject and group analyses could be performed. Source localization procedures revealed that the N2pc is composed of two distinct neural responses, an early parietal source (180-200 ms) and a later occipito-temporal source (220-240 ms). These findings are consistent with the proposal that parietal areas are used to initiate a shift of attention within a visual search array and that the focusing of attention is implemented by extrastriate areas of the occipital and inferior temporal cortex.     

The detection of contingency and animacy from simple animations in the human brain

Contingencies between objects and people can be mechanical or intentional-social in nature. In this fMRI study we used simplified stimuli to investigate brain regions involved in the detection of mechanical and intentional contingencies. Using a factorial design we manipulated the 'animacy' and 'contingency' of stimulus movement, and the subject's attention to the contingencies. The detection of mechanical contingency between shapes whose movement was inanimate engaged the middle temporal gyrus and right intraparietal sulcus. The detection of intentional contingency between shapes whose movement was animate activated superior parietal networks bilaterally. These activations were unaffected by attention to contingency. Additional regions, the right middle frontal gyrus and left superior temporal sulcus, became activated by the animate-contingent stimuli when subjects specifically attended to the contingent nature of the stimuli. Our results help to clarify neural networks previously associated with 'theory of mind' and agency detection. In particular, the results suggest that low-level perception of agency in terms of objects reacting to other objects at a distance is processed by parietal networks. In contrast, the activation of brain regions traditionally associated with theory of mind tasks appears to require attention to be directed towards agency and contingency.     

Consequences of magnocellular dysfunction on processing attended information in schizophrenia

Schizophrenia is associated with perceptual and cognitive dysfunction including impairments in visual attention. These impairments may be related to deficits in early stages of sensory/perceptual processing, particularly within the magnocellular/dorsal visual pathway. In the present study, subjects viewed high and low spatial frequency (SF) gratings designed to test functioning of the parvocellular/magnocellular pathways, respectively. Schizophrenia patients and healthy controls attended to either the low SF (magnocellularly biased) or high SF (parvocellularly biased) gratings. Functional magnetic resonance imaging (fMRI) and recordings of event-related potentials (ERPs) were carried out during task performance. Patients were impaired at detecting low-frequency targets. ERP amplitudes to low-frequency gratings were diminished, both for the early sensory-evoked components and for the attend minus unattend difference component (the selection negativity), which is regarded as a neural index of feature-selective attention. Similarly, fMRI revealed that activity in extrastriate visual cortex was reduced in patients during attention to low, but not high, SF. In contrast, activity in frontal and parietal areas, previously implicated in the control of attention, did not differ between patients and controls. These findings suggest that impaired sensory processing of magnocellularly biased stimuli lead to impairments in the effective processing of attended stimuli, even when the attention control systems themselves are intact.     

Retinotopic organization in human visual cortex and the spatial precision of functional MRI

A method of using functional magnetic resonance imaging (fMRI) to measure retinotopic organization within human cortex is described. The method is based on a visual stimulus that creates a traveling wave of neural activity within retinotopically organized visual areas. We measured the fMRI signal caused by this stimulus in visual cortex and represented the results on images of the flattened cortical sheet. We used the method to locate visual areas and to evaluate the spatial precision of fMRI. Specifically, we: (i) identified the borders between several retinotopically organized visual areas in the posterior occipital lobe; (ii) measured the function relating cortical position to visual field eccentricity within area V1; (iii) localized activity to within 1.1 mm of visual cortex; and (iv) estimated the spatial resolution of the fMRI signal and found that signal amplitude falls to 60% at a spatial frequency of 1 cycle per 9 mm of visual cortex. This spatial resolution is consistent with a linespread whose full width at half maximum spreads across 3.5 mm of visual cortex.      

Tactile attention tasks enhance activation in somatosensory regions of parietal cortex: a positron emission tomography study.

We used positron emission tomography to study cortical regions mediating tactile attention. Cues selectively directed subjects to attend to the roughness or duration of contact with embossed gratings that rubbed against a single fingertip with controlled speed and force. The task required discriminating between paired gratings that differed in tactile features of roughness and/or length. For different blocks of trials, cues directed attention to one tactile feature or indicated a divided attention strategy to a change in either feature. All attention conditions unambiguously activated several somatosensory foci in the parietal cortex, including somatotopically appropriate portions of the primary somatosensory cortex in the postcentral gyrus (S1) and the secondary somatosensory region (S2) within parietal opercular regions. There was no evidence for separate processing foci for selective and divided attention strategies, or for selectively attending to roughness versus stimulus duration. We observed a greater magnitude blood flow change in S2 versus S1 during attention tasks, which suggests that S2 might actually influence S1 activity. Despite these differences, modulation of S1 and S2 supports concepts of early selection in tactile attention. There were also examples of non-sensory foci in frontal cortex, anterior cingulate gyrus and bilateral superior parietal regions at the fundus of the postcentral sulcus. Posterior parietal regions observed in this study did not overlap foci seen in studies of visual attention. Thus, the posterior parietal region may be subdivided into modality-specific subregions, each of which processes information needed to attend to a specific modality. These non-sensory areas may constitute a network that provides a source of modulating influences on the earlier stage, sensory areas.     

Source analysis of event-related cortical activity during visuo-spatial attention

Recordings of event-related potentials (ERPs) were combined with structural and functional magnetic resonance imaging (fMRI) to study the spatio-temporal patterns of cortical activity that underlie visual-spatial attention. Small checkerboard stimuli were flashed in random order to the four quadrants of the visual field at a rapid rate while subjects attended to stimuli in one quadrant at a time. Attended stimuli elicited enhanced ERP components in the latency range 80-200 ms that were co-localized with fMRI activations in multiple extrastriate cortical regions. The earliest ERP component (C1 at 50-90 ms) was unaffected by attention and was localized by dipole modeling to calcarine cortex. A longer latency deflection in the 150-225 ms range that was accounted for by this same calcarine source, however, did show consistent modulation with attention. This late attention effect, like the C1, inverted in polarity for upper versus lower field stimuli, consistent with a neural generator in primary visual cortex (area V1). These results provide support to current hypotheses that spatial attention in humans is associated with delayed feedback to area V1 from higher extrastriate areas that may have the function of improving the salience of stimuli at attended locations.     

Spontaneous activity associated with primary visual cortex: a resting-state FMRI study

Brain functions during the resting state have attracted considerable attention in the past several years. However, little has been known about spontaneous activity in the sensory cortices in the task-free state. This study used functional magnetic resonance imaging (fMRI) to investigate the existence of spontaneous activity in the primary visual areas (PVA) of normal-sighted subjects and to explore the physiological implications of such activity. Our results revealed that we were able to detect spontaneous activity, which was nonrandom in that it was distinctly clustered both temporally and spatially in the PVA of each subject. In addition, the neural network associated with the PVA-related spontaneous activity included the visual association areas, the precuneus, the precentral/postcentral gyrus, the middle frontal gyrus, the fusiform gyrus, the inferior/middle temporal gyrus, and the parahippocampal gyrus. After considering the functions of these regions, we speculated that the PVA-related spontaneous activity may be associated with memory-related mental imagery and/or visual memory consolidation processes. These findings confirm the presence of spontaneous activity in the PVA and related brain areas. This confirmation supports the perspective that brain is a system intrinsically operating on its own, and sensory information interacts with rather than determines the operation of the system.     

Category-specific conceptual processing of color and form in left fronto-temporal cortex

To investigate the cortical basis of color and form concepts, we examined event-related functional magnetic resonance imaging (fMRI) responses to matched words related to abstract color and form information. Silent word reading elicited activity in left temporal and frontal cortex, where category-specific activity differences were also observed. Whereas color words preferentially activated anterior parahippocampal gyrus, form words evoked category-specific activity in fusiform and middle temporal gyrus as well as premotor and dorsolateral prefrontal areas in inferior and middle frontal gyri. These results demonstrate that word meanings and concepts are not processed by a unique cortical area, but by different sets of areas, each of which may contribute differentially to conceptual semantic processing. We hypothesize that the anterior parahippocampal activation to color words indexes computation of the visual feature conjunctions and disjunctions necessary for classifying visual stimuli under a color concept. The predominant premotor and prefrontal activation to form words suggests action-related information processing and may reflect the involvement of neuronal elements responding in an either-or fashion to mirror neurons related to adumbrating shapes.     

Neural basis for priming of pop-out during visual search revealed with fMRI

Maljkovic and Nakayama first showed that visual search efficiency can be influenced by priming effects. Even "pop-out" targets (defined by unique color) are judged quicker if they appear at the same location and/or in the same color as on the preceding trial, in an unpredictable sequence. Here, we studied the potential neural correlates of such priming in human visual search using functional magnetic resonance imaging (fMRI). We found that repeating either the location or the color of a singleton target led to repetition suppression of blood oxygen level-dependent (BOLD) activity in brain regions traditionally linked with attentional control, including bilateral intraparietal sulci. This indicates that the attention system of the human brain can be "primed," in apparent analogy to repetition-suppression effects on activity in other neural systems. For repetition of target color but not location, we also found repetition suppression in inferior temporal areas that may be associated with color processing, whereas repetition of target location led to greater reduction of activation in contralateral inferior parietal and frontal areas, relative to color repetition. The frontal eye fields were also implicated, notably when both target properties (color and location) were repeated together, which also led to further BOLD decreases in anterior fusiform cortex not seen when either property was repeated alone. These findings reveal the neural correlates for priming of pop-out search, including commonalities, differences, and interactions between location and color repetition. fMRI repetition-suppression effects may arise in components of the attention network because these settle into a stable "attractor state" more readily when the same target property is repeated than when a different attentional state is required.     

The functional neuroanatomy of novelty processing: integrating ERP and fMRI results.

Recent research indicates that non-tonal novel events, deviating from an ongoing auditory environment, elicit a positive event-related potential (ERP), the novel P3. Although a variety of studies examined the neural network engaged in novelty detection, there is no complete picture of the underlying brain mechanisms. This experiment investigated these neural mechanisms by combining ERP and functional magnetic resonance imaging (fMRI). Hemodynamic and electrophysiological responses were measured in the same subjects using the same experimental design. The ERP analysis revealed a novel P3, while the fMRI responses showed bilateral foci in the middle part of the superior temporal gyrus. When subjects attended to the novel stimuli only identifiable novel sounds evoked a N4-like negativity. Subjects showing a strong N4-effect had additional fMRI activation in right prefrontal cortex (rPFC) as compared to subjects with a weak N4-effect. This pattern of results suggests that novelty processing not only includes the registration of deviancy but may also lead to a fast access and retrieval of related semantic concepts. The fMRI activation pattern suggests that the superior temporal gyrus is involved in novelty detection, whereas accessing and retrieving semantic concepts related to novel sounds additionally engages the rPFC.     

Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus

We studied the existence, localization and attentional modulation of gamma-band oscillatory activity (30-130 Hz) in the human intracranial region. Two areas known to play a key role in visual object processing: the lateral occipital (LO) cortex and the fusiform gyrus. These areas consistently displayed large gamma oscillations during visual stimulus encoding, while other extrastriate areas remained systematically silent, across 14 patients and 291 recording sites scattered throughout extrastriate visual cortex. The lateral extent of the responsive regions was small, in the range of 5 mm. Induced gamma oscillations and evoked potentials were not systematically co-localized. LO and the fusiform gyrus displayed markedly different patterns of attentional modulation. In the fusiform gyrus, attention enhanced stimulus-driven gamma oscillations. In LO, attention increased the baseline level of gamma oscillations during the expectation period preceding the stimulus. Subsequent gamma oscillations produced by attended stimuli were smaller than those produced by unattended, irrelevant stimuli. Attentional modulations of gamma oscillations in LO and the fusiform gyrus were thus very different, both in their time-course (preparatory period and/or stimulus processing) and direction of modulation (increase or decrease). Our results thus suggest that the functional role of gamma oscillations depends on the area in which they occur.     

Enhanced temporal non-linearities in human object-related occipito-temporal cortex

To what extent does neural activation in human visual cortex follow the temporal dynamics of the optical retinal stimulus? Specifically, to what extent does stimulus evoked neural activation persist after stimulus termination? In the present study, we used functional magnetic resonance imaging (fMRI) to explore the resulting temporal non-linearities across the entire constellation of human visual areas. Gray-scale images of animals, houses and faces were presented at two different presentation rates - 1 and 4 Hz - and the fMRI signal was analyzed in retinotopic and in high order occipito-temporal visual areas. In early visual areas and the motion sensitive area MT/V5, a fourfold increase in stimulus presentation rate evoked a twofold increase in signal amplitude. However, in high order visual areas, signal amplitude increased only by 25%. A control experiment ruled out the possibility that this difference was due to signal saturation ('ceiling') effects. A likely explanation for the stronger non-linearities in occipito-temporal cortex is a persistent neuronal activation that continues well after stimulus termination in the 1 Hz condition. These persistent activations might serve as a short term (iconic) memory mechanism for preserving a trace of the stimulus even in its absence and for future integration with temporally correlated stimuli. Two alternative models of persistence (inhibitory and excitatory) are proposed to explain the data.     

Ongoing brain activity fluctuations directly account for intertrial and indirectly for intersubject variability in Stroop task performance

Recent studies have established a relation between ongoing brain activity fluctuations and intertrial variability in evoked neural responses, perception, and motor performance. Here, we extended these investigations into the domain of cognitive control. Using functional neuroimaging and a sparse event-related design (with long and unpredictable intervals), we measured ongoing activity fluctuations and evoked responses in volunteers performing a Stroop task with color-word interference. Across trials, prestimulus activity of several regions predicted subsequent response speed and across subjects this effect scaled with the Stroop effect size, being significant only in subjects manifesting behavioral interference. These effects occurred only in task relevant as the dorsal anterior cingulate and dorsolateral prefrontal cortex as well as ventral visual areas sensitive to color and visual words. Crucially, in subjects showing a Stroop effect, reaction times were faster when prestimulus activity was higher in task-relevant (color) regions and slower when activity was higher in irrelevant (word form) regions. These findings suggest that intrinsic brain activity fluctuations modulate neural mechanisms underpinning selective voluntary attention and cognitive control. Rephrased in terms of predictive coding models, ongoing activity can hence be considered a proxy of the precision (gain) with which prediction error signals are transmitted upon sensory stimulation.