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.     

Mapping of contextual modulation in the population response of primary visual cortex

We review the evidence of long-range contextual modulation in V1. Populations of neurons in V1 are activated by a wide variety of stimuli outside of their classical receptive fields (RF), well beyond their surround region. These effects generally involve extra-RF features with an orientation component. The population mapping of orientation preferences to the upper layers of V1 is well understood, as far as the classical RF properties are concerned, and involves organization into pinwheel-like structures. We introduce a novel hypothesis regarding the organization of V1’s contextual response. We show that RF and extra-RF orientation preferences are mapped in related ways. Orientation pinwheels are the foci of both types of features. The mapping of contextual features onto the orientation pinwheel has a form that recapitulates the organization of the visual field: an iso-orientation patch within the pinwheel also responds to extra-RF stimuli of the same orientation. We hypothesize that the same form of mapping applies to other stimulus properties that are mapped out in V1, such as colour and contrast selectivity. A specific consequence is that fovea-like properties will be mapped in a systematic way to orientation pinwheels. We review the evidence that cytochrome oxidase blobs comprise the foci of this contextual remapping for colour and low contrasts. Neurodynamics and motion in the visual field are argued to play an important role in the shaping and maintenance of this type of mapping in V1.     

Changes in visual receptive fields with microstimulation of frontal cortex

The influence of attention on visual cortical neurons has been described in terms of its effect on the structure of receptive fields (RFs), where multiple stimuli compete to drive neural responses and ultimately behavior. We stimulated the frontal eye field (FEF) of passively fixating monkeys and produced changes in V4 responses similar to known effects of voluntary attention. Subthreshold FEF stimulation enhanced visual responses at particular locations within the RF and altered the interaction between pairs of RF stimuli to favor those aligned with the activated FEF site. Thus, we could influence which stimulus drove the responses of individual V4 neurons. These results suggest that spatial signals involved in saccade preparation are used to covertly select among multiple stimuli appearing within the RFs of visual cortical neurons.     

Feature-based attention in the frontal eye field and area V4 during visual search

When we search for a target in a crowded visual scene, we often use the distinguishing features of the target, such as color or shape, to guide our attention and eye movements. To investigate the neural mechanisms of feature-based attention, we simultaneously recorded neural responses in the frontal eye field (FEF) and area V4 while monkeys performed a visual search task. The responses of cells in both areas were modulated by feature attention, independent of spatial attention, and the magnitude of response enhancement was inversely correlated with the number of saccades needed to find the target. However, an analysis of the latency of sensory and attentional influences on responses suggested that V4 provides bottom-up sensory information about stimulus features, whereas the FEF provides a top-down attentional bias toward target features that modulates sensory processing in V4 and that could be used to guide the eyes to a searched-for target.     

Interacting roles of attention and visual salience in V4

Attention increases the contrast gain of V4 neurons, causing them to respond to an attended stimulus as though its contrast had increased. When multiple stimuli appear within a neuron's receptive field (RF), the neuron responds primarily to the attended stimulus. This suggests that cortical cells may be "hard wired" to respond preferentially to the highest-contrast stimulus in their RF, and neural systems for attention capitalize on this mechanism by dynamically increasing the effective contrast of the stimulus that is task relevant. To test this, we varied the relative contrast of two stimuli within the recorded neurons' RFs, while the monkeys attended away to another location. Increasing the physical contrast of one stimulus caused V4 neurons to respond preferentially to that stimulus and reduced their responses to competing stimuli. When attention was directed to the lower-contrast stimulus, it partially overcame the influence of a competing, higher-contrast stimulus.     

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.     

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.     

Modulation of V1 Spike Response by Temporal Interval of Spatiotemporal Stimulus Sequence

The spike activity of single neurons of the primary visual cortex (V1) becomes more selective and reliable in response to wide-field natural scenes compared to smaller stimuli confined to the classical receptive field (RF). However, it is largely unknown what aspects of natural scenes increase the selectivity of V1 neurons. One hypothesis is that modulation by surround interaction is highly sensitive to small changes in spatiotemporal aspects of RF surround. Such a fine-tuned modulation would enable single neurons to hold information about spatiotemporal sequences of oriented stimuli, which extends the role of V1 neurons as a simple spatiotemporal filter confined to the RF. In the current study, we examined the hypothesis in the V1 of awake behaving monkeys, by testing whether the spike response of single V1 neurons is modulated by temporal interval of spatiotemporal stimulus sequence encompassing inside and outside the RF. We used two identical Gabor stimuli that were sequentially presented with a variable stimulus onset asynchrony (SOA): the preceding one (S1) outside the RF and the following one (S2) in the RF. This stimulus configuration enabled us to examine the spatiotemporal selectivity of response modulation from a focal surround region. Although S1 alone did not evoke spike responses, visual response to S2 was modulated for SOA in the range of tens of milliseconds. These results suggest that V1 neurons participate in processing spatiotemporal sequences of oriented stimuli extending outside the RF.     

P50 Sensory Gating in Infants

Attentional deficits are common in a variety of neuropsychiatric disorders including attention deficit-hyperactivity disorder, autism, bipolar mood disorder, and schizophrenia. There has been increasing interest in the neurodevelopmental components of these attentional deficits; neurodevelopmental meaning that while the deficits become clinically prominent in childhood or adulthood, the deficits are the results of problems in brain development that begin in infancy or even prenatally. Despite this interest, there are few methods for assessing attention very early in infancy. This report focuses on one method, infant auditory P50 sensory gating.Attention has several components. One of the earliest components of attention, termed sensory gating, allows the brain to tune out repetitive, noninformative sensory information. Auditory P50 sensory gating refers to one task designed to measure sensory gating using changes in EEG. When identical auditory stimuli are presented 500 ms apart, the evoked response (change in the EEG associated with the processing of the click) to the second stimulus is generally reduced relative to the response to the first stimulus (i.e. the response is "gated"). When response to the second stimulus is not reduced, this is considered a poor sensory gating, is reflective of impaired cerebral inhibition, and is correlated with attentional deficits.Because the auditory P50 sensory gating task is passive, it is of potential utility in the study of young infants and may provide a window into the developmental time course of attentional deficits in a variety of neuropsychiatric disorders. The goal of this presentation is to describe the methodology for assessing infant auditory P50 sensory gating, a methodology adapted from those used in studies of adult populations.     

The role of attention in visual processing

Attention to a visual stimulus typically increases the responses of cortical neurons to that stimulus. Because many studies have shown a close relationship between the performance of individual neurons and behavioural performance of animal subjects, it is important to consider how attention affects this relationship. Measurements of behavioural and neuronal performance taken from rhesus monkeys while they performed a motion detection task with two attentional states show that attention alters the relationship between behaviour and neuronal response. Notably, attention affects the relationship differently in different cortical visual areas. This indicates that a close relationship between neuronal and behavioural performance on a given task persists over changes in attentional state only within limited regions of visual cortex.     

Foraging strategy switching in an antlion larva

Prepulse inhibition (PPI) refers to the process wherein startle responses to salient stimuli (e.g., startling sound pulses) are attenuated by the presentation of another stimulus (e.g., a brief pre-pulse) immediately before the startling stimulus. Accordingly, deficits in PPI reflect atypical sensorimotor gating that is linked to neurobehavioral systems underlying responsivity to emotionally evocative cues. Little is known about the effects of changes in visual contextual information in PPI among humans. In this study, the effects of introducing unexpected changes in the visual scenes presented on a computer monitor on the human auditory startle response and PPI were assessed in young adults. Based on our animal data showing that unexpected transitions from a dark to a light environment reduce the startle response and PPI in rats after the illumination transition, it was hypothesized that novel changes in visual scenes would produce similar effects in humans. Results show that PPI decreased when elements were added to or removed from visual scenes, and that this effect declined after repeated presentations of the modified scene, supporting the interpretation that the PPI reduction was due to novel information being processed. These findings are the first to demonstrate that novel visual stimuli can impair sensorimotor gating of auditory stimuli in humans.     

Independent genetic loci for sensorimotor gating and attentional performance in BXD recombinant inbred strains

A startle reflex in response to an intense acoustic stimulus is inhibited when a barely detectable pulse precedes the startle stimulus by 30-500 ms. It has been theorized that this phenomenon, named prepulse inhibition (PPI) of a startle response, is an automatic early-stage gating process contributing to the ability to focus attention. Deficits in PPI may therefore contribute to deficits in attentional processing. Both deficits are observed in schizophrenia spectrum disorders. Here, we investigated whether there is overlap in genetic control of PPI and attentional processing phenotypes in the panel of BXD recombinant inbred strains of mice. Using an individually titrated prepulse intensity to handle differences in perceived prepulse intensities among strains, we identified a significant quantitative trait locus (QTL) for PPI at the mid-distal end of chromosome 17. A measure of attentional processing in the five-choice serial reaction time task, response variability, mapped to a different locus on proximal-mid chromosome 16. In addition, the estimated genetic and environmental correlations between PPI and several attentional phenotypes were low and not significant. Taken together, the observation of separate genetic loci for PPI and attention and the absence of genetic and environmental correlations indicate that differences in sensorimotor gating do not contribute to differences in attentional performance. Therefore, it is worth pursuing the causative genes residing in both attention and PPI QTL, as these may contribute to separate molecular pathways implicated in neuropsychiatric diseases, such as schizophrenia.     

Specific contributions of ventromedial, anterior cingulate, and lateral prefrontal cortex for attentional selection and stimulus valuation

Attentional control ensures that neuronal processes prioritize the most relevant stimulus in a given environment. Controlling which stimulus is attended thus originates from neurons encoding the relevance of stimuli, i.e. their expected value, in hand with neurons encoding contextual information about stimulus locations, features, and rules that guide the conditional allocation of attention. Here, we examined how these distinct processes are encoded and integrated in macaque prefrontal cortex (PFC) by mapping their functional topographies at the time of attentional stimulus selection. We find confined clusters of neurons in ventromedial PFC (vmPFC) that predominantly convey stimulus valuation information during attention shifts. These valuation signals were topographically largely separated from neurons predicting the stimulus location to which attention covertly shifted, and which were evident across the complete medial-to-lateral extent of the PFC, encompassing anterior cingulate cortex (ACC), and lateral PFC (LPFC). LPFC responses showed particularly early-onset selectivity and primarily facilitated attention shifts to contralateral targets. Spatial selectivity within ACC was delayed and heterogeneous, with similar proportions of facilitated and suppressed responses during contralateral attention shifts. The integration of spatial and valuation signals about attentional target stimuli was observed in a confined cluster of neurons at the intersection of vmPFC, ACC, and LPFC. These results suggest that valuation processes reflecting stimulus-specific outcome predictions are recruited during covert attentional control. Value predictions and the spatial identification of attentional targets were conveyed by largely separate neuronal populations, but were integrated locally at the intersection of three major prefrontal areas, which may constitute a functional hub within the larger attentional control network.     

Decoding seen and attended motion directions from activity in the human visual cortex

Functional neuroimaging has successfully identified brain areas that show greater responses to visual motion and adapted responses to repeated motion directions. However, such methods have been thought to lack the sensitivity and spatial resolution to isolate direction-selective responses to individual motion stimuli. Here, we used functional magnetic resonance imaging (fMRI) and pattern classification methods to show that ensemble activity patterns in human visual cortex contain robust direction-selective information, from which it is possible to decode seen and attended motion directions. Ensemble activity in areas V1-V4 and MT+/V5 allowed us to decode which of eight possible motion directions the subject was viewing on individual stimulus blocks. Moreover, ensemble activity evoked by single motion directions could effectively predict which of two overlapping motion directions was the focus of the subject's attention and presumably dominant in perception. Our results indicate that feature-based attention can bias direction-selective population activity in multiple visual areas, including MT+/V5 and early visual areas (V1-V4), consistent with gain-modulation models of feature-based attention and theories of early attentional selection. Our approach for measuring ensemble direction selectivity may provide new opportunities to investigate relationships between attentional selection, conscious perception, and direction-selective responses in the human brain.     

Alpha ERD and human visual selective attention

We compared the alpha band EEG depression (event-related desynchnization, ERD) level in two tasks, involving activation of different attentional processes: visual search for a deviant relevant stimulus among many similar ones and visual oddball. Control data for the visual search task consisted of simple viewing of several stimuli being of the same shape as the relevant stimulus in the search trials. Gaze position was verified by eye tracking method. We interpreted alpha band ERD as a correlate of activation of attentional processes. Fixating the target in visual search task caused a significantly larger ERD than fixating the same stimuli in control trials over all leads. We suppose this to be related with task and visual environment complexities. The frontal ERD domination may indicate attentional control over voluntary movements execution (top-down attention). The caudal ERD may be related with updating of visual information as a result of search process (bottom-up attention). Both relevant and irrelevant stimuli in the oddball task also induced alpha band ERD, but it was larger in response to relevant one and reached maximum level over occipital leads. Domination of caudal ERD in oddball task is supposed to indicate bottom-up attention processes.     

Distribution of attention modulates salience signals in early visual cortex

Previous research has shown that the extent to which people spread attention across the visual field plays a crucial role in visual selection and the occurrence of bottom-up driven attentional capture. Consistent with previous findings, we show that when attention was diffusely distributed across the visual field while searching for a shape singleton, an irrelevant salient color singleton captured attention. However, while using the very same displays and task, no capture was observed when observers initially focused their attention at the center of the display. Using event-related fMRI, we examined the modulation of retinotopic activity related to attentional capture in early visual areas. Because the sensory display characteristics were identical in both conditions, we were able to isolate the brain activity associated with exogenous attentional capture. The results show that spreading of attention leads to increased bottom-up exogenous capture and increased activity in visual area V3 but not in V2 and V1.     

Covariation between Spike and LFP Modulations Revealed with Focal and Asynchronous Stimulation of Receptive Field Surround in Monkey Primary Visual Cortex

A focal visual stimulus outside the classical receptive field (RF) of a V1 neuron does not evoke a spike response by itself, and yet evokes robust changes in the local field potential (LFP). This subthreshold LFP provides a unique opportunity to investigate how changes induced by surround stimulation leads to modulation of spike activity. In the current study, two identical Gabor stimuli were sequentially presented with a variable stimulus onset asynchrony (SOA) ranging from 0 to 100 ms: the first (S1) outside the RF and the second (S2) over the RF of primary visual cortex neurons, while trained monkeys performed a fixation task. This focal and asynchronous stimulation of the RF surround enabled us to analyze the modulation of S2-evoked spike activity and covariation between spike and LFP modulation across SOA. In this condition, the modulation of S2-evoked spike response was dominantly facilitative and was correlated with the change in LFP amplitude, which was pronounced for the cells recorded in the upper cortical layers. The time course of covariation between the SOA-dependent spike modulation and LFP amplitude suggested that the subthreshold LFP evoked by the S1 can predict the magnitude of upcoming spike modulation.     

Changes in receptive field of tectal neurons evoked by vestibular and acoustic stimulation in pigeons

Responses to visual, acoustic, and vestibular stimuli were studied in neurons of the middle and deep layers of the tectum in the pigeon. Changes in the receptive field (RF) were assessed from comparison of unit responses to isolated movement of a shaped visual stimulus with responses to movement of a stimulus during simultaneous action of a vestibular or acoustic stimulus. Changes in RF of the neuron could be observed during the action of both a vestibular and an acoustic stimulus. These changes affected the identification of the predominant direction of movement of the stimulus, the position of the maximum in the response histogram, and the duration and number of spikes in the response. The direction of change in RF of the neuron was found not necessarily to coincide with the sign of the response to the same neuron to isolated presentation of a vestibular or acoustic stimulus. It is postulated on the basis of the results and data in the literature that the tectum transforms the flow of impulses arriving from the retina depending on the nature of the information received by it from other sensory systems.     

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.