Topographic maps of visual spatial attention in human parietal cortex

Functional magnetic resonance imaging (fMRI) was used to measure activity in human parietal cortex during performance of a visual detection task in which the focus of attention systematically traversed the visual field. Critically, the stimuli were identical on all trials (except for slight contrast changes in a fully randomized selection of the target locations) whereas only the cued location varied. Traveling waves of activity were observed in posterior parietal cortex consistent with shifts in covert attention in the absence of eye movements. The temporal phase of the fMRI signal in each voxel indicated the corresponding visual field location. Visualization of the distribution of temporal phases on a flattened representation of parietal cortex revealed at least two distinct topographically organized cortical areas within the intraparietal sulcus (IPS), each representing the contralateral visual field. Two cortical areas were proposed based on this topographic organization, which we refer to as IPS1 and IPS2 to indicate their locations within the IPS. This nomenclature is neutral with respect to possible homologies with well-established cortical areas in the monkey brain. The two proposed cortical areas exhibited relatively little response to passive visual stimulation in comparison with early visual areas. These results provide evidence for multiple topographic maps in human parietal cortex.     

Neuronal correlates of perception in early visual cortex

We used functional magnetic resonance imaging (fMRI) to measure activity in human early visual cortex (areas V1, V2 and V3) during a challenging contrast-detection task. Subjects attempted to detect the presence of slight contrast increments added to two kinds of background patterns. Behavioral responses were recorded so that the corresponding cortical activity could be grouped into the usual signal detection categories: hits, false alarms, misses and correct rejects. For both kinds of background patterns, the measured cortical activity was retinotopically specific. Hits and false alarms were associated with significantly more cortical activity than were correct rejects and misses. That false alarms evoked more activity than misses indicates that activity in early visual cortex corresponded to the subjects' percepts, rather than to the physically presented stimulus.     

Enhanced visual spatial attention ipsilateral to rTMS-induced 'virtual lesions' of human parietal cortex

The breakdown of attentional mechanisms after brain damage can have drastic behavioral consequences, as in patients suffering from spatial neglect. While much research has concentrated on impaired attention to targets contralateral to sites of brain damage, here we report the ipsilateral enhancement of visual attention after repetitive transcranial magnetic stimulation (rTMS) of parietal cortex at parameters known to reduce cortical excitability. Normal healthy subjects received rTMS (1 Hz, 10 mins) over right or left parietal cortex. Subsequently, detection of visual stimuli contralateral to the stimulated hemisphere was consistently impaired when stimuli were also present in the opposite hemifield, mirroring the extinction phenomenon commonly observed in neglect patients. Additionally, subjects' attention to ipsilateral targets improved significantly over normal levels. These results underline the potential of focal brain dysfunction to produce behavioral improvement and give experimental support to models of interhemispheric competition in the distributed brain network for spatial attention.     

Neural correlates of age-related decline and compensation in visual attention capacity

We identified neural correlates of declined and preserved basic visual attention functions in aging individuals based on Bundesen “Theory of Visual Attention”. In an interindividual difference approach, we contrasted electrophysiology of higher- and lower-performing younger and older participants. In both age groups, the same distinct components indexed performance levels of parameters visual processing speed C and visual short-term memory storage capacity K. The posterior N1 marked interindividual differences in C and the contralateral delay activity marked interindividual differences in K. Moreover, both parameters were selectively related to 2 further event-related potential waves in older age. The anterior N1 was reduced for older participants with lower processing speed, indicating that age-related loss of attentional resources slows encoding. An enhanced right-central positivity was found only for older participants with high storage capacity, suggesting compensatory recruitment for retaining visual short-term memory performance. Together, our results demonstrate that attentional capacity in older age depends on both preservation and successful reorganization of the underlying brain circuits.     

Global effects of feature-based attention in human visual cortex

The content of visual experience depends on how selective attention is distributed in the visual field. We used functional magnetic resonance imaging (fMRI) in humans to test whether feature-based attention can globally influence visual cortical responses to stimuli outside the attended location. Attention to a stimulus feature (color or direction of motion) increased the response of cortical visual areas to a spatially distant, ignored stimulus that shared the same feature.     

Object-based attention to one of two superimposed surfaces alters responses in human early visual cortex

Faced with an overwhelming amount of sensory information, we are able to prioritize the processing of select spatial locations and visual features. The neuronal mechanisms underlying such spatial and feature-based selection have been studied in considerable detail. More recent work shows that attention can also be allocated to objects, even spatially superimposed objects composed of dynamically changing features that must be integrated to create a coherent object representation. Much less is known about the mechanisms underlying such object-based selection. Our goal was to investigate behavioral and neuronal responses when attention was directed to one of two objects, specifically one of two superimposed transparent surfaces, in a task designed to preclude space-based and feature-based selection. We used functional magnetic resonance imaging (fMRI) to measure changes in blood oxygen level-dependent (BOLD) signals when attention was deployed to one or the other surface. We found that visual areas V1, V2, V3, V3A, and MT+ showed enhanced BOLD responses to translations of an attended relative to an unattended surface. These results reveal that visual areas as early as V1 can be modulated by attending to objects, even objects defined by dynamically changing elements. This provides definitive evidence in humans that early visual areas are involved in a seemingly high-order process. Furthermore, our results suggest that these early visual areas may participate in object-specific feature "binding," a process that seemingly must occur for an object or a surface to be the unit of attentional selection.     

Neural correlates of the automatic and goal-driven biases in orienting spatial attention

How do stimuli in the environment interact with the goals of observers? We addressed this question by showing that the relevance of an abruptly appearing visual object (cue) changes how observers orient attention toward a subsequent object (target) and how this target is represented in the activity of neurons in the superior colliculus. Initially after the appearance of the cue, attention is driven to its locus. This capture of attention is followed by a second bias in orienting attention, where observers preferentially orient to new locations in the visual scene-an effect called inhibition of return. In the superior colliculus, these two automatic biases in orienting attention were associated with changes in neural activity linked to the appearance of the target-relatively stronger activity linked to the capture of attention and weaker activity linked to inhibition of return. This behavioral pattern changes when the cue predicts the upcoming location of the target-the benefit associated with the capture of attention is enhanced and inhibition of return is reduced. These goal-driven changes in behavior were associated with an increase in pretarget- and target-related activity. Taken together, the goals of observers modify stimulus-driven changes in neural activity with both signals represented in the salience maps of the superior colliculi.     

Influences of lesions of parietal cortex on visual spatial attention in humans

Summary Several brain areas have been identified with attention, because damage to these regions leads to neglect and extinction. We have tested elements of visual attentional processing in patients with parietal, frontal, or temporal lesions and compared their responses to control subjects. Normal humans respond faster in a reaction time task when the spatial location of a target is correctly predicted by an antecedent stimulus (valid cue) than when the location is incorrectly predicted (invalid cue). The cue is hypothesized to shift attention towards its location and thereby facilitate or impede response latencies. The reaction times of individuals with damage to the parietal lobe are somewhat slowed for targets ipsilateral or contralateral to the side of the lesion if the targets are preceded by valid cues. These same patients are extremely slow in responding to targets in the visual field contralateral to the lesion when the cue has just appeared in the unaffected (ipsilateral) visual field. In addition, these individuals are especially slow in responding to targets in either visual field when the lights are preceded by weak, diffuse illumination of the entire visual field. Patients with lesions of the frontal lobe have very slow reaction times in general and, as is the case for patients with lesions of the temporal lobe, are slow in all conditions for targets in the field contralateral to the lesion. These patterns are probably not associated with attentional defects. For patients with parietal lesions, these studies demonstrate a further deficit in a cued reaction-time task suggesting abnormal visual attention. Since different sites of brain damage yield different patterns of responses, tests such as these could be of analytic and diagnostic value.     

Modulations of early somatosensory ERP components by transient and sustained spatial attention

To investigate when and how spatial attention affects somatosensory processing, event-related brain potentials (ERPs) were recorded in response to mechanical tactile stimuli delivered to the left and right hand while attention was directed to one of these hands. The attended hand either remained constant throughout an experimental block (sustained attention), or was changed across successive trials (transient attention). Attentional modulations of the N140 component and a sustained 'processing negativity' for attended stimuli were observed in both attention conditions. However, attentional effects on earlier somatosensory components differed systematically. Sustained attention resulted in a contralateral negativity overlapping with the N80 component, while transient attention was reflected by a bilateral positivity overlapping with the P100 component. This dissociation indicates that sustained and transient attention affect different somatosensory areas. It is suggested that sustained attention can modulate tactile processing within primary somatosensory cortex (S1), while effects of transient attention are located beyond S1. Overall, results demonstrate that spatial selectivity in touch is mediated by activity modulations in modality-specific somatosensory cortex.     

Neural correlates of spatial orienting in the human superior colliculus

A natural visual scene contains more information than the visual system has the capacity to simultaneously process, requiring specific items to be selected for detailed analysis at the expense of others. Such selection and inhibition are fundamental in guiding search behavior, but the neural basis of these mechanisms remains unclear. Abruptly appearing visual items can automatically capture attention, but once attention has been directed away from the salient event, return to that same location is slowed. In non-human primates, signals associated with attentional capture (AC) and subsequent inhibition of return (IOR) have been recorded from the superior colliculus (SC)--a structure known to play a pivotal role in reflexive spatial orienting. Here, we sought to establish whether similar signals could be recorded from the human SC, as well as early retinotopic cortical visual areas, where signals associated with AC and IOR have yet to be investigated with respect to oculomotor responses. Using an optimized oculomotor paradigm together with high-field, high-spatial resolution functional magnetic resonance imaging and high-speed eye tracking, we demonstrate that BOLD signal changes recorded from the human SC correlate strongly with our saccadic measures of AC and IOR. A qualitatively similar pattern of responses was found for V1, but only the inhibitory response associated with IOR persisted through V2 and V3. Although the SC plays a role in mediating these automatic attentional biasing signals, the source of these signals is likely to lie in higher cortical areas.     

Neural coding of global form in the human visual cortex

Extensive psychophysical and computational work proposes that the perception of coherent and meaningful structures in natural images relies on neural processes that convert information about local edges in primary visual cortex to complex object features represented in the temporal cortex. However, the neural basis of these mid-level vision mechanisms in the human brain remains largely unknown. Here, we examine functional MRI (fMRI) selectivity for global forms in the human visual pathways using sensitive multivariate analysis methods that take advantage of information across brain activation patterns. We use Glass patterns, parametrically varying the perceived global form (concentric, radial, translational) while ensuring that the local statistics remain similar. Our findings show a continuum of integration processes that convert selectivity for local signals (orientation, position) in early visual areas to selectivity for global form structure in higher occipitotemporal areas. Interestingly, higher occipitotemporal areas discern differences in global form structure rather than low-level stimulus properties with higher accuracy than early visual areas while relying on information from smaller but more selective neural populations (smaller voxel pattern size), consistent with global pooling mechanisms of local orientation signals. These findings suggest that the human visual system uses a code of increasing efficiency across stages of analysis that is critical for the successful detection and recognition of objects in complex environments.     

Spatial and cross-modal attention alter responses to unattended sensory information in early visual and auditory human cortex

Attending to a visual or auditory stimulus often requires irrelevant information to be filtered out, both within the modality attended and in other modalities. For example, attentively listening to a phone conversation can diminish our ability to detect visual events. We used functional magnetic resonance imaging (fMRI) to examine brain responses to visual and auditory stimuli while subjects attended visual or auditory information. Although early cortical areas are traditionally considered unimodal, we found that brain responses to the same ignored information depended on the modality attended. In early visual area V1, responses to ignored visual stimuli were weaker when attending to another visual stimulus, compared with attending to an auditory stimulus. The opposite was true in more central visual area MT+, where responses to ignored visual stimuli were weaker when attending to an auditory stimulus. Furthermore, fMRI responses to the same ignored visual information depended on the location of the auditory stimulus, with stronger responses when the attended auditory stimulus shared the same side of space as the ignored visual stimulus. In early auditory cortex, responses to ignored auditory stimuli were weaker when attending a visual stimulus. A simple parameterization of our data can describe the effects of redirecting attention across space within the same modality (spatial attention) or across modalities (cross-modal attention), and the influence of spatial attention across modalities (cross-modal spatial attention). Our results suggest that the representation of unattended information depends on whether attention is directed to another stimulus in the same modality or the same region of space.     

Neuronal correlates of signal detection in the posterior parietal cortex of rats performing a sustained attention task

The posterior parietal cortex (PPC) plays an integral role in visuospatial attention. Evidence suggests that neuronal activity in the PPC predicts the allocation of attention to stimuli. The present experiment tested the hypothesis that in rats performing a sustained attention task, the detection of signals, as opposed to missed signals, is associated with increased PPC unit activity. Single unit activity was recorded from the PPC of rats and analyzed individually and as a population vector for each recording session. A population of single units (28/111) showed significant activation evoked by signals on trials resulting in correct performance (hits). A smaller population of neurons (three/111) was activated on trials in which signals were not detected by the animals (misses). Analysis of populations of simultaneously recorded neurons indicated increased activation predicting signal detection; no population of neurons was activated on trials in which the animal incorrectly pressed the hit lever following nonsignals. The increased, hit-predicting activity was not modulated by signal duration or the presence of a visual distractor, although the distractor reduced the number of trials in which hit-predicting activity and subsequent correct detection occurred. These findings indicate that attentional signal processing in the PPC integrates successful detection of signals.     

Transient neural activity in human parietal cortex during spatial attention shifts

Observers viewing a complex visual scene selectively attend to relevant locations or objects and ignore irrelevant ones. Selective attention to an object enhances its neural representation in extrastriate cortex, compared with those of unattended objects, via top-down attentional control signals. The posterior parietal cortex is centrally involved in this control of spatial attention. We examined brain activity during attention shifts using rapid, event-related fMRI of human observers as they covertly shifted attention between two peripheral spatial locations. Activation in extrastriate cortex increased after a shift of attention to the contralateral visual field and remained high during sustained contralateral attention. The time course of activity was substantially different in posterior parietal cortex, where transient increases in activation accompanied shifts of attention in either direction. This result suggests that activation of the parietal cortex is associated with a discrete signal to shift spatial attention, and is not the source of a signal to continuously maintain the current attentive state.     

Subcortical gating in the human visual system during spatial selective attention

The question of whether subcortical gating occurs as a function of spatial selective attention remains unsettled. This issue was investigated, using the paradigm of Eason et al. (1969) wherein subjects are instructed to attend to a specified location in a given visual field while attempting to ignore stimuli presented in the opposite field. Visual evoked responses falling within the 40-70 ms range were found to be significantly more negative when the location at which the evoking stimulus appeared was being attended to than when it was not. Also, later deflections (100-200 ms) were enhanced in amplitude and negatively biased. The very early effect provides further evidence for spatial attention-induced precortical gating. The later effects provide additional evidence for the amplitude enhancement of 'exogenous' components, along with the possible involvement of glial cell activity in the generation of slow wave negativity.     

Neural correlates of priming on occluded figure interpretation in human fusiform cortex

The visual system rapidly completes a partially occluded figure. We probed the completion process by using priming in combination with neuroimaging techniques. Priming leads to more efficient visual processing and thus a reduction in neural activity in relevant brain areas. These areas were studied with high spatial resolution and temporal accuracy with focus on early perceptual processing. We recorded magnetoencephalographic responses from 10 human volunteers in a primed same-different task for test figures. The test figures were preceded by a sequence of two figures, a prime or control figure followed by an occluded figure. The prime figures were one of three possible interpretations of the occluded figures: global and local completions and mosaic interpretation. A significant priming effect was evident: in primed trials as compared with control trials, subjects responded faster and the latency was shorter in the magnetoencephalographic signal for the largest peak between 50 and 300 ms after the occluded figure onset. Tomographic and statistical parametric mapping analyses revealed stages of activation in occipitotemporal areas during occluded figure processing. Notably, we found significantly reduced activation in the right fusiform cortex between 120 and 200 ms after occluded figure onset for primed trials as compared with control trials. We also found significant spatiotemporal differences of local, global and mosaic interpretations for individual subjects but not across subjects. We conclude that modulation of activity in the right fusiform cortex may be a neural correlate of priming in the interpretation of an occluded figure, and that this area acts as a hub for different occluded figure interpretations in this early stage of perception.     

Neural mechanisms of visual selective attention

Visual selective attention improves our perception and performance by modifying sensory inputs at an early stage of processing. Spatial attention produces the most consistent early modulations of visual processing, which can be observed when attention is voluntarily allocated to locations. These effects of spatial attention are similar when attention is cued in a trial-by-trial, or sustained, fashion and are manifest as changes in the amplitudes, but not the latencies, of evoked neural activity recorded from the intact human scalp. This modulation of sensory processing first occurs within the extrastriate visual cortex and not within the striate or earlier subcortical processing stages. These relatively early spatial filters alter the inputs to higher stages of visual analysis that are responsible for feature extraction and ultimately object perception and recognition, and thus provide physiological evidence for early precategorical selection during visual attention. Moreover, the physiological evidence extends early selection theories by providing neurophysiologically precise information about the stages of visual processing affected by attention.     

Predictive coding for motion stimuli in human early visual cortex

The current study investigates if early visual cortical areas, V1, V2 and V3, use predictive coding to process motion information. Previous studies have reported biased visual motion responses at locations where novel visual information was presented (i.e., the motion trailing edge), which is plausibly linked to the predictability of visual input. Using high-field functional magnetic resonance imaging (fMRI), we measured brain activation during predictable versus unpreceded motion-induced contrast changes during several motion stimuli. We found that unpreceded moving dots appearing at the trailing edge gave rise to enhanced BOLD responses, whereas predictable moving dots at the leading edge resulted in suppressed BOLD responses. Furthermore, we excluded biases in directional sensitivity, shifts in cortical stimulus representation, visuo-spatial attention and classical receptive field effects as viable alternative explanations. The results clearly indicate the presence of predictive coding mechanisms in early visual cortex for visual motion processing, underlying the construction of stable percepts out of highly dynamic visual input.     

Activation of the visual cortex in motivated attention

Functional activation (measured with fMRI) in occipital cortex was more extensive when participants view pictures strongly related to primary motive states (i.e., victims of violent death, viewer-directed threat, and erotica). This functional activity was greater than that observed for less intense emotional (i.e., happy families or angry faces) or neutral images (i.e., household objects, neutral faces). Both the extent and strength of functional activity were related to the judged affective arousal of the different picture contents, and the same pattern of functional activation was present whether pictures were presented in color or in grayscale. It is suggested that more extensive visual system activation reflects "motivated attention," in which appetitive or defensive motivational engagement directs attention and facilitates perceptual processing of survival-relevant stimuli.     

Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency

We report here that shape-from-shading stimuli evoked a long-latency contextual pop-out response in V1 and V2 neurons of macaque monkeys, particularly after the monkeys had used the stimuli in a behavioral task. The magnitudes of the pop-out responses were correlated to the monkeys' behavioral performance, suggesting that these signals are neural correlates of perceptual pop-out saliency. The signals changed with the animal's behavioral adaptation to stimulus contingencies, indicating that perceptual saliency is also a function of experience and behavioral relevance. The evidence that higher-order stimulus attributes and task experience can influence early visual processing supports the notion that perceptual computation is an interactive and plastic process involving multiple cortical areas.