Modulation of activity in human visual area V1 during memory masking

Neurons in the primary visual cortex, V1, are specialized for the processing of elemental features of the visual stimulus, such as orientation and spatial frequency. Recent fMRI evidence suggest that V1 neurons are also recruited in visual perceptual memory; a number of studies using multi-voxel pattern analysis have successfully decoded stimulus-specific information from V1 activity patterns during the delay phase in memory tasks. However, consistent fMRI signal modulations reflecting the memory process have not yet been demonstrated. Here, we report evidence, from three subjects, that the low V1 BOLD activity during retention of low-level visual features is caused by competing interactions between neural populations coding for different values along the spectrum of the dimension remembered. We applied a memory masking paradigm in which the memory representation of a masker stimulus interferes with a delayed spatial frequency discrimination task when its frequency differs from the discriminanda with ±1 octave and found that impaired behavioral performance due to masking is reflected in weaker V1 BOLD signals. This cross-channel inhibition in V1 only occurs with retinotopic overlap between the masker and the sample stimulus of the discrimination task. The results suggest that memory for spatial frequency is a local process in the retinotopically organized visual cortex.     

Attentional modulations related to spatial gating but not to allocation of limited resources in primate V1

Attention can modulate neural responses in sensory cortical areas and improve behavioral performance in perceptual tasks. However, the nature and purpose of these modulations remain under debate. Here we?used voltage-sensitive dye imaging (VSDI) to measure V1 population responses while monkeys performed a difficult detection task under focal or distributed attention. We found that V1 responses at attended locations are significantly elevated relative to actively ignored or irrelevant locations, consistent with the hypothesis that an important goal of attention in V1 is to highlight task-relevant information. Surprisingly, these modulations were indistinguishable under focal and distributed attention, suggesting a minor or no role for attention as a mechanism for allocating limited representational resources in V1. The response elevation at attended locations is additive, is widespread, and starts shortly before stimulus onset. This elevation could contribute to spatial gating by biasing competition in subsequent processing stages in favor of attended stimuli.     

Human cortical mechanisms of visual attention during orienting and search.

Functional anatomical studies indicate that a set of neural signals in parietal and frontal cortex mediates the covert allocation of attention to visual locations across a wide variety of visual tasks. This frontoparietal network includes areas, such as the frontal eye field and supplementary eye field. This anatomical overlap suggests that shifts of attention to visual locations of objects recruit areas involved in oculomotor programming and execution. Finally, the fronto-parietal network may be the source of spatial attentional modulations in the ventral visual system during object recognition or discrimination.     

The role of attention in figure-ground segregation in areas V1 and V4 of the visual cortex

Our visual system segments images into objects and background. Figure-ground segregation relies on the detection of feature discontinuities that signal boundaries between the figures and the background and on a complementary region-filling process that groups together image regions with similar features. The neuronal mechanisms for these processes are not well understood and it is unknown how they depend on visual attention. We measured neuronal activity in V1 and V4 in a task where monkeys either made an eye movement to texture-defined figures or ignored them. V1 activity predicted the timing and the direction of the saccade if the figures were task relevant. We found that boundary detection is an early process that depends little on attention, whereas region filling occurs later and is facilitated by visual attention, which acts in an object-based manner. Our findings are explained by a model with local, bottom-up computations for boundary detection and feedback processing for region filling.     

Attention-dependent representation of a size illusion in human V1

One of the most fundamental properties of human primary visual cortex (V1) is its retinotopic organization, which makes it an ideal candidate for encoding spatial properties, such as size, of objects. However, three-dimensional (3D) contextual information can lead to size illusions that are reflected in the spatial pattern of activity in V1 [1]. A critical question is how complex 3D contextual information can influence spatial activity patterns in V1. Here, we assessed whether changes in the spatial distribution of activity in V1 depend on the focus of attention, which would be suggestive of feedback of 3D contextual information from higher visual areas. We presented two 3D rings at close and far apparent depths in a 3D scene. When subjects fixated its center, the far ring appeared to be larger and occupy a more eccentric portion of the visual field, relative to the close ring. Using functional magnetic resonance imaging, we found that the spatial distribution of V1 activity induced by the far ring was also shifted toward a more eccentric representation of the visual field, whereas that induced by the close ring was shifted toward the foveal representation, consistent with their perceptual appearances. This effect was significantly reduced when the focus of spatial attention was narrowed with a demanding central fixation task. We reason that focusing attention on the fixation task resulted in reduced activity in--and therefore reduced feedback from--higher visual areas that process the 3D depth cues.     

Spatial and Feature-Based Attention in a Layered Cortical Microcircuit Model

Directing attention to the spatial location or the distinguishing feature of a visual object modulates neuronal responses in the visual cortex and the stimulus discriminability of subjects. However, the spatial and feature-based modes of attention differently influence visual processing by changing the tuning properties of neurons. Intriguingly, neurons'' tuning curves are modulated similarly across different visual areas under both these modes of attention. Here, we explored the mechanism underlying the effects of these two modes of visual attention on the orientation selectivity of visual cortical neurons. To do this, we developed a layered microcircuit model. This model describes multiple orientation-specific microcircuits sharing their receptive fields and consisting of layers 2/3, 4, 5, and 6. These microcircuits represent a functional grouping of cortical neurons and mutually interact via lateral inhibition and excitatory connections between groups with similar selectivity. The individual microcircuits receive bottom-up visual stimuli and top-down attention in different layers. A crucial assumption of the model is that feature-based attention activates orientation-specific microcircuits for the relevant feature selectively, whereas spatial attention activates all microcircuits homogeneously, irrespective of their orientation selectivity. Consequently, our model simultaneously accounts for the multiplicative scaling of neuronal responses in spatial attention and the additive modulations of orientation tuning curves in feature-based attention, which have been observed widely in various visual cortical areas. Simulations of the model predict contrasting differences between excitatory and inhibitory neurons in the two modes of attentional modulations. Furthermore, the model replicates the modulation of the psychophysical discriminability of visual stimuli in the presence of external noise. Our layered model with a biologically suggested laminar structure describes the basic circuit mechanism underlying the attention-mode specific modulations of neuronal responses and visual perception.     

Errors Disrupt Subsequent Early Attentional Processes

It has been demonstrated that target detection is impaired following an error in an unrelated flanker task. These findings support the idea that the occurrence or processing of unexpected error-like events interfere with subsequent information processing. In the present study, we investigated the effect of errors on early visual ERP components. We therefore combined a flanker task and a visual discrimination task. Additionally, the intertrial interval between both tasks was manipulated in order to investigate the duration of these negative after-effects. The results of the visual discrimination task indicated that the amplitude of the N1 component, which is related to endogenous attention, was significantly decreased following an error, irrespective of the intertrial interval. Additionally, P3 amplitude was attenuated after an erroneous trial, but only in the long-interval condition. These results indicate that low-level attentional processes are impaired after errors.     

Spatial cueing,sensory gating and selective response preparation: an ERP study on visuo-spatial orienting

Event-related brain potentials (ERPs) were recorded in a visuo-spatial attention task where the position of an imperative stimulus was indicated either validly or invalidly by a central arrow (trial-by-trial cueing). Subjects had to perform choice RT tasks with the response being dependent either on the identity of the target stimulus or on its position. When target identity was relevant for response selection, validly cued stimuli elicited amplitude enhancements of the early, sensory-evoked P1 and N1 components at lateral posterior sites. The N1 validity effect was limited to scalp sites ipsilateral to the visual field of stimulus presentation. Although these effects were found only when the sensory discrimination task was considerably difficult, they are in line with models assuming that modulations of sensory-perceptual processing (“sensory gating”) are induced by spatial cueing. However, when target location was response-relevant, N1 amplitude enhancements were consistently elicited by invalidly cued letters.CNV and LRP measures indicated that the arrow elicited response-related processing in the cue-target interval. Such processes occurred even when the cue contained no information about an upcoming response. Two consecutive lateralization phases were distinguishable in the LRP, with experimentally induced response assignments becoming effective only during the second phase.     

Binocular Flash Suppression in the Primary Visual Cortex of Anesthetized and Awake Macaques

Primary visual cortex (V1) was implicated as an important candidate for the site of perceptual suppression in numerous psychophysical and imaging studies. However, neurophysiological results in awake monkeys provided evidence for competition mainly between neurons in areas beyond V1. In particular, only a moderate percentage of neurons in V1 were found to modulate in parallel with perception with magnitude substantially smaller than the physical preference of these neurons. It is yet unclear whether these small modulations are rooted from local circuits in V1 or influenced by higher cognitive states. To address this question we recorded multi-unit spiking activity and local field potentials in area V1 of awake and anesthetized macaque monkeys during the paradigm of binocular flash suppression. We found that a small but significant modulation was present in both the anesthetized and awake states during the flash suppression presentation. Furthermore, the relative amplitudes of the perceptual modulations were not significantly different in the two states. We suggest that these early effects of perceptual suppression might occur locally in V1, in prior processing stages or within early visual cortical areas in the absence of top-down feedback from higher cognitive stages that are suppressed under anesthesia.     

Perceptual organization of local elements into global shapes in the human visual cortex

The question of how local image features on the retina are integrated into perceived global shapes is central to our understanding of human visual perception. Psychophysical investigations have suggested that the emergence of a coherent visual percept, or a "good-Gestalt", is mediated by the perceptual organization of local features based on their similarity. However, the neural mechanisms that mediate unified shape perception in the human brain remain largely unknown. Using human fMRI, we demonstrate that not only higher occipitotemporal but also early retinotopic areas are involved in the perceptual organization and detection of global shapes. Specifically, these areas showed stronger fMRI responses to global contours consisting of collinear elements than to patterns of randomly oriented local elements. More importantly, decreased detection performance and fMRI activations were observed when misalignment of the contour elements disturbed the perceptual coherence of the contours. However, grouping of the misaligned contour elements by disparity resulted in increased performance and fMRI activations, suggesting that similar neural mechanisms may underlie grouping of local elements to global shapes by different visual features (orientation or disparity). Thus, these findings provide novel evidence for the role of both early feature integration processes and higher stages of visual analysis in coherent visual perception.     

Attentional demands of movement observation as tested by a dual task approach

Movement observation (MO) has been shown to activate the motor cortex of the observer as indicated by an increase of corticomotor excitability for muscles involved in the observed actions. Moreover, behavioral work has strongly suggested that this process occurs in a near-automatic manner. Here we further tested this proposal by applying transcranial magnetic stimulation (TMS) when subjects observed how an actor lifted objects of different weights as a single or a dual task. The secondary task was either an auditory discrimination task (experiment 1) or a visual discrimination task (experiment 2). In experiment 1, we found that corticomotor excitability reflected the force requirements indicated in the observed movies (i.e. higher responses when the actor had to apply higher forces). Interestingly, this effect was found irrespective of whether MO was performed as a single or a dual task. By contrast, no such systematic modulations of corticomotor excitability were observed in experiment 2 when visual distracters were present. We conclude that interference effects might arise when MO is performed while competing visual stimuli are present. However, when a secondary task is situated in a different modality, neural responses are in line with the notion that the observers motor system responds in a near-automatic manner. This suggests that MO is a task with very low cognitive demands which might be a valuable supplement for rehabilitation training, particularly, in the acute phase after the incident or in patients suffering from attention deficits. However, it is important to keep in mind that visual distracters might interfere with the neural response in M1.     

A Feedback Model of Attention Explains the Diverse Effects of Attention on Neural Firing Rates and Receptive Field Structure

Visual attention has many effects on neural responses, producing complex changes in firing rates, as well as modifying the structure and size of receptive fields, both in topological and feature space. Several existing models of attention suggest that these effects arise from selective modulation of neural inputs. However, anatomical and physiological observations suggest that attentional modulation targets higher levels of the visual system (such as V4 or MT) rather than input areas (such as V1). Here we propose a simple mechanism that explains how a top-down attentional modulation, falling on higher visual areas, can produce the observed effects of attention on neural responses. Our model requires only the existence of modulatory feedback connections between areas, and short-range lateral inhibition within each area. Feedback connections redistribute the top-down modulation to lower areas, which in turn alters the inputs of other higher-area cells, including those that did not receive the initial modulation. This produces firing rate modulations and receptive field shifts. Simultaneously, short-range lateral inhibition between neighboring cells produce competitive effects that are automatically scaled to receptive field size in any given area. Our model reproduces the observed attentional effects on response rates (response gain, input gain, biased competition automatically scaled to receptive field size) and receptive field structure (shifts and resizing of receptive fields both spatially and in complex feature space), without modifying model parameters. Our model also makes the novel prediction that attentional effects on response curves should shift from response gain to contrast gain as the spatial focus of attention drifts away from the studied cell.     

Attention to stimulus features shifts spectral tuning of V4 neurons during natural vision

Previous neurophysiological studies suggest that attention can alter the baseline or gain of neurons in extrastriate visual areas but that it cannot change tuning. This suggests that neurons in visual cortex function as labeled lines whose meaning does not depend on task demands. To test this common assumption, we used a system identification approach to measure spatial frequency and orientation tuning in area V4 during two attentionally demanding visual search tasks, one that required fixation and one that allowed free viewing during search. We found that spatial attention modulates response baseline and gain but does not alter tuning, consistent with previous reports. In contrast, feature-based attention often shifts neuronal tuning. These tuning shifts are inconsistent with the labeled-line model and tend to enhance responses to stimulus features that distinguish the search target. Our data suggest that V4 neurons behave as matched filters that are dynamically tuned to optimize visual search.     

Expectation Suppression in Early Visual Cortex Depends on Task Set

Stimulus expectation can modulate neural responses in early sensory cortical regions, with expected stimuli often leading to a reduced neural response. However, it is unclear whether this expectation suppression is an automatic phenomenon or is instead dependent on the type of task a subject is engaged in. To investigate this, human subjects were presented with visual grating stimuli in the periphery that were either predictable or non-predictable while they performed three tasks that differently engaged cognitive resources. In two of the tasks, the predictable stimulus was task-irrelevant and spatial attention was engaged at fixation, with a high load on either perceptual or working memory resources. In the third task, the predictable stimulus was task-relevant, and therefore spatially attended. We observed that expectation suppression is dependent on the cognitive resources engaged by a subjects’ current task. When the grating was task-irrelevant, expectation suppression for predictable items was visible in retinotopically specific areas of early visual cortex (V1-V3) during the perceptual task, but it was abolished when working memory was loaded. When the grating was task-relevant and spatially attended, there was no significant effect of expectation in early visual cortex. These results suggest that expectation suppression is not an automatic phenomenon, but dependent on attentional state and type of available cognitive resources.     

Preparatory effects of distractor suppression: evidence from visual cortex

Spatial selective attention is the mechanism that facilitates the selection of relevant information over irrelevant information in the visual field. The current study investigated whether foreknowledge of the presence or absence of distractors surrounding an impending target stimulus results in preparatory changes in visual cortex. We cued the location of the target and the presence or absence of distractors surrounding the target while changes in blood oxygen level dependent (BOLD) signals were measured. In line with prior work, we found that top-down spatial attention resulted in an increased contralateral BOLD response, evoked by the cue throughout early visual cortex (areas V1, V2 and V3). In addition, cues indicating distractor presence evoked a substantial increase in the magnitude of the BOLD signal in visual area V3, but not in V2 or V1. This study shows that prior knowledge concerning the presence of a distractor results in enhanced attentional modulation of visual cortex, in visual areas where neuronal receptive fields are large enough to encompass both targets and distractors. We interpret these findings as evidence that top-down attentional control processes include active preparatory suppression mechanisms for irrelevant, distracting information in the visual scene.     

Set-size effects for spatial frequency change and discrimination in multiple targets

In visual search tasks with a near-threshold target amongst distracters, log detection thresholds rise in proportion to the log of the number of stimuli. Previous research has shown a very steep slope for this set-size effect where the target is a change in spatial frequency (SF) across an ISI, suggesting a low-level explanation for 'change blindness (Wright et al., 2000). Here, we analyse stimulus and task variables in order to determine the contributions of stimulus detection and attention processes. Stimuli consisted of two 150 ms frames each containing 1 to 4 Gabor targets, with an ISI of 250 ms. In a 2AFC detection task with uniform distracters, slopes of 0.23-0.52 were found, in line with visual search results. 2AFC SF discrimination tasks gave slopes of 0.68, 0.69 with homogeneous distracters and 0.76-0.96 with inhomogeneous distracters, consistent with averaging of stimuli within a frame. If the distracters were also made to change across ISI, averaging was impossible, and focal attention was required to solve the discrimination. This always gave set-size slopes > 1. It is concluded that, under conditions where a stimulus array can be analysed globally, change detection performance is limited by signal detection mechanisms, rather than limited capacity attention or memory mechanisms. However, where this is prevented, for example by changing more than one item, limitations due to attention or memory produce an even steeper set-size effect.     

A human extrastriate area functionally homologous to macaque V4

Extrastriate area V4 is crucial for intermediate form vision and visual attention in nonhuman primates. Human neuroimaging suggests that an area in the lingual sulcus/fusiform gyrus may correspond to ventral V4 (V4v). We studied a human neurological patient, AR, with a putative V4v lesion. The lesion does not affect early visual processing (luminance, orientation, and motion perception). However, it does impair hue perception, intermediate form vision, and visual attention in the upper contralateral visual field. Form deficits occur during discrimination of illusory borders, Glass patterns, curvature, and non-Cartesian patterns. Attention deficits occur during discrimination of the relative positions of object parts, detection of low-salience targets, and orientation discrimination in the presence of distractors. This pattern of deficits is consistent with the known properties of area V4 in nonhuman primates, indicating that AR's lesion affects a cortical region functionally homologous to macaque V4.     

Dissociable influences of auditory object vs. spatial attention on visual system oscillatory activity

Given that both auditory and visual systems have anatomically separate object identification ("what") and spatial ("where") pathways, it is of interest whether attention-driven cross-sensory modulations occur separately within these feature domains. Here, we investigated how auditory "what" vs. "where" attention tasks modulate activity in visual pathways using cortically constrained source estimates of magnetoencephalograpic (MEG) oscillatory activity. In the absence of visual stimuli or tasks, subjects were presented with a sequence of auditory-stimulus pairs and instructed to selectively attend to phonetic ("what") vs. spatial ("where") aspects of these sounds, or to listen passively. To investigate sustained modulatory effects, oscillatory power was estimated from time periods between sound-pair presentations. In comparison to attention to sound locations, phonetic auditory attention was associated with stronger alpha (7-13 Hz) power in several visual areas (primary visual cortex; lingual, fusiform, and inferior temporal gyri, lateral occipital cortex), as well as in higher-order visual/multisensory areas including lateral/medial parietal and retrosplenial cortices. Region-of-interest (ROI) analyses of dynamic changes, from which the sustained effects had been removed, suggested further power increases during Attend Phoneme vs. Location centered at the alpha range 400-600 ms after the onset of second sound of each stimulus pair. These results suggest distinct modulations of visual system oscillatory activity during auditory attention to sound object identity ("what") vs. sound location ("where"). The alpha modulations could be interpreted to reflect enhanced crossmodal inhibition of feature-specific visual pathways and adjacent audiovisual association areas during "what" vs. "where" auditory attention.     

Characterizing visual performance fields: effects of transient covert attention, spatial frequency, eccentricity, task and set size

We investigated whether transient covert attention would differentially affect 'performance fields' (shape depicted by percent correct performance at particular locations in the visual field) for orientation discrimination, detection and localization tasks, while manipulating a number of visual factors. We found that although attention improved overall performance, it did not affect performance fields. Two patterns were observed regardless of the presence of a local post-mask, the stimulus orientation, or the task. A horizontal-vertical anisotropy (HVA) became more pronounced as spatial frequency, eccentricity and set size increased. A vertical meridian asymmetry (VMA) became more pronounced as spatial frequency and eccentricity increased. We conclude that performance fields are determined by visual, rather than by transient attentional, constraints.     

Auditory Attention Activates Peripheral Visual Cortex

Background

Recent neuroimaging studies have revealed that putatively unimodal regions of visual cortex can be activated during auditory tasks in sighted as well as in blind subjects. However, the task determinants and functional significance of auditory occipital activations (AOAs) remains unclear.

Methodology/Principal Findings

We examined AOAs in an intermodal selective attention task to distinguish whether they were stimulus-bound or recruited by higher-level cognitive operations associated with auditory attention. Cortical surface mapping showed that auditory occipital activations were localized to retinotopic visual cortex subserving the far peripheral visual field. AOAs depended strictly on the sustained engagement of auditory attention and were enhanced in more difficult listening conditions. In contrast, unattended sounds produced no AOAs regardless of their intensity, spatial location, or frequency.

Conclusions/Significance

Auditory attention, but not passive exposure to sounds, routinely activated peripheral regions of visual cortex when subjects attended to sound sources outside the visual field. Functional connections between auditory cortex and visual cortex subserving the peripheral visual field appear to underlie the generation of AOAs, which may reflect the priming of visual regions to process soon-to-appear objects associated with unseen sound sources.