Transcranial magnetic stimulation to frontal but not occipital cortex disrupts endogenous attention.

Covert endogenous (voluntary) attention improves visual performance. Human neuroimaging studies suggest that the putative human homolog of macaque frontal eye fields (FEF+) is critical for this improvement, whereas early visual areas are not. Yet, correlational MRI methods do not manipulate brain function. We investigated whether rFEF+ or V1/V2 plays a causal role in endogenous attention. We used transcranial magnetic stimulation (TMS) to alter activity in the visual cortex or rFEF+ when observers performed an orientation discrimination task while attention was manipulated. On every trial, they received double-pulse TMS at a predetermined site (stimulated region) around V1/V2 or rFEF+. Two cortically magnified gratings were presented, one in the stimulated region (contralateral to the stimulated area) and another in the symmetric (ipsilateral) nonstimulated region. Grating contrast was varied to measure contrast response functions (CRFs) for all attention and stimulation combinations. In experiment 1, the CRFs were similar at the stimulated and nonstimulated regions, indicating that early visual areas do not modulate endogenous attention during stimulus presentation. In contrast, occipital TMS eliminates exogenous (involuntary) attention effects on performance [A. Fernández, M. Carrasco,Curr. Biol. 30, 4078-4084 (2020)]. In experiment 2, rFEF+ stimulation decreased the overall attentional effect; neither benefits at the attended location nor costs at the unattended location were significant. The frequency and directionality of microsaccades mimicked this pattern: Whereas occipital stimulation did not affect microsaccades, rFEF+ stimulation caused a higher microsaccade rate directed toward the stimulated hemifield. These results provide causal evidence of the role of this frontal region for endogenous attention.

Presaccadic Attention Depends on Eye Movement Direction and Is Related to V1 Cortical Magnification.

With every saccadic eye movement, humans bring new information into their fovea to be processed with high visual acuity. Notably, perception is enhanced already before a relevant item is foveated: During saccade preparation, presaccadic attention shifts to the upcoming fixation location, which can be measured via behavioral correlates such as enhanced visual performance or modulations of sensory feature tuning. The coupling between saccadic eye movements and attention is assumed to be robust and mandatory and considered a mechanism facilitating the integration of pre- and postsaccadic information. However, until recently it had not been investigated as a function of saccade direction. Here, we measured contrast response functions during fixation and saccade preparation in male and female observers and found that the pronounced response gain benefit typically elicited by presaccadic attention is selectively lacking before upward saccades at the group level-some observers even showed a cost. Individual observer's sensitivity before upward saccades was negatively related to their amount of surface area in primary visual cortex representing the saccade target, suggesting a potential compensatory mechanism that optimizes the use of the limited neural resources processing the upper vertical meridian. Our results raise the question of how perceptual continuity is achieved and how upward saccades can be accurately targeted despite the lack of-theoretically required-presaccadic attention.

A dynamic 1/f noise protocol to assess visual attention without biasing perceptual processing.

Psychophysical paradigms measure visual attention via localized test items to which observers must react or whose features have to be discriminated. These items, however, potentially interfere with the intended measurement, as they bias observers' spatial and temporal attention to their location and presentation time. Furthermore, visual sensitivity for conventional test items naturally decreases with retinal eccentricity, which prevents direct comparison of central and peripheral attention assessments. We developed a stimulus that overcomes these limitations. A brief oriented discrimination signal is seamlessly embedded into a continuously changing 1/f noise field, such that observers cannot anticipate potential test locations or times. Using our new protocol, we demonstrate that local orientation discrimination accuracy for 1/f filtered signals is largely independent of retinal eccentricity. Moreover, we show that items present in the visual field indeed shape the distribution of visual attention, suggesting that classical studies investigating the spatiotemporal dynamics of visual attention via localized test items may have obtained a biased measure. We recommend our protocol as an efficient method to evaluate the behavioral and neurophysiological correlates of attentional orienting across space and time.

The effect of spatial structure on presaccadic attention costs and benefits assessed with dynamic 1/f noise.

Already before the onset of a saccadic eye movement, we preferentially process visual information at the upcoming eye fixation. This 'presaccadic shift of attention' is typically assessed via localized test items, which potentially bias the attention measurement. Here we show how presaccadic attention shapes perception from saccade origin to target when no scene-structuring items are presented. Participants made saccades into a 1/f ('pink') noise field, in which we embedded a brief orientation signal at various locations shortly before saccade onset. Local orientation discrimination performance served as a proxy for the allocation of attention. Results demonstrate that (1) the presaccadic attention shift is accompanied by considerable attentional costs at the presaccadic eye fixation; (2) saccades are preceded by shifts of attention to their goal location even if they are directed into an unstructured visual field, but the spread of attention, compared to target-directed saccades, is broad; We conclude that the absence or presence of saccade target objects markedly shapes the distribution of presaccadic attention, and likely the underlying (space-based or object-based) cortical control mechanism. Our findings demonstrate the relevance of an item-free approach for measuring attentional dynamics across the visual field.

Visual attention is not limited to the oculomotor range.

Both patients with eye movement disorders and healthy participants whose oculomotor range had been experimentally reduced have been reported to show attentional deficits at locations unreachable by their eyes. Whereas previous studies were mainly based on the evaluation of reaction times, we measured visual sensitivity before saccadic eye movements and during fixation at locations either within or beyond participants' oculomotor range. Participants rotated their heads to prevent them from performing large rightward saccades. In this posture, an attentional cue was presented inside or outside their oculomotor range. Participants either made a saccade to the cue or maintained fixation while they discriminated the orientation of a visual noise patch. In contrast to previous reports, we found that the cue attracted visual attention regardless of whether it was presented within or beyond participants' oculomotor range during both fixation and saccade preparation. Moreover, when participants aimed to look to a cue that they could not reach with their eyes, we observed no benefit at their actual saccade endpoint. This demonstrates that spatial attention is not coupled to the executed oculomotor program but instead can be deployed unrestrictedly also toward locations to which no saccade can be executed. Our results are compatible with the view that covert and overt attentional orienting are guided by feedback projections of visual and visuomotor neurons of the gaze control system, irrespective of oculomotor limitations.

Visual attention and eye movement control during oculomotor competition.

Saccadic eye movements are typically preceded by selective shifts of visual attention. Recent evidence, however, suggests that oculomotor selection can occur in the absence of attentional selection when saccades erroneously land in between nearby competing objects (saccade averaging). This study combined a saccade task with a visual discrimination task to investigate saccade target selection during episodes of competition between a saccade target and a nearby distractor. We manipulated the spatial predictability of target and distractor locations and asked participants to execute saccades upon variably delayed go-signals. This allowed us to systematically investigate the capacity to exert top-down eye movement control (as reflected in saccade endpoints) based on the spatiotemporal dynamics of visual attention during movement preparation (measured as visual sensitivity). Our data demonstrate that the predictability of target and distractor locations, despite not affecting the deployment of visual attention prior to movement preparation, largely improved the accuracy of short-latency saccades. Under spatial uncertainty, a short go-signal delay likewise enhanced saccade accuracy substantially, which was associated with a more selective deployment of attentional resources to the saccade target. Moreover, we observed a systematic relationship between the deployment of visual attention and saccade accuracy, with visual discrimination performance being significantly enhanced at the saccade target relative to the distractor only before the execution of saccades accurately landing at the saccade target. Our results provide novel insights linking top-down eye movement control to the operation of selective visual attention during movement preparation.

Opposite Dynamics of GABA and Glutamate Levels in the Occipital Cortex during Visual Processing.

Magnetic resonance spectroscopy (MRS) measures the two most common inhibitory and excitatory neurotransmitters, GABA and glutamate, in the human brain. However, the role of MRS-derived GABA and glutamate signals in relation to system-level neural signaling and behavior is not fully understood. In this study, we investigated levels of GABA and glutamate in the visual cortex of healthy human participants (both genders) in three functional states with increasing visual input. Compared with a baseline state of eyes closed, GABA levels decreased after opening the eyes in darkness and Glx levels remained stable during eyes open but increased with visual stimulation. In relevant states, GABA and Glx correlated with amplitude of fMRI signal fluctuations. Furthermore, visual discriminatory performance correlated with the level of GABA, but not Glx. Our study suggests that differences in brain states can be detected through the contrasting dynamics of GABA and Glx, which has implications in interpreting MRS measurements.SIGNIFICANCE STATEMENT GABA and glutamate are the two most abundant neurotransmitters in human brain. Their interaction, known as inhibitory-excitatory balance, plays a crucial role in establishing spontaneous and stimulus-driven brain activity. Yet, the relationship between magnetic resonance spectroscopy (MRS)-derived levels of both metabolites and fMRI is still a matter of dispute. In this work, we study GABA and glutamate in three states of visual processing and in relation to fMRI and visual discriminatory performance in healthy people. We found that states of visual processing can be detected through the contrasting dynamics of GABA and glutamate and their correlation with fMRI signals. We also demonstrated that GABA, but not glutamate, in the visual system predicts visual performance. Our results provide insights into MRS-derived GABA and glutamate measurements.

Sensitivity measures of visuospatial attention.

Measuring visual sensitivity has become popular to determine the spatial deployment of visual attention. Critically, the accuracy of the measurement depends on the quality of the stimulus used. We evaluated the strengths and weaknesses of six commonly used stimuli for assessing visual attention. While preparing an eye movement to a cued item, participants discriminated a stimulus-specific visual feature, either at the cued location or at other equidistant uncued locations. Stimuli differed in their visual features (digital letters, Gabors, crosses, pink noise, random dot kinematograms, and Gabor streams) and their presentation mode (static or dynamic stimuli). We evaluated these stimuli regarding their temporal and spatial specificity and their impact on saccade preparation. We assessed presaccadic visual sensitivity as a correlate of visual spatial attention and discuss the stimulus-specific time course, spatial specificity, and magnitude of the measured attention modulation. Irrespective of the stimulus type, we observed a clear increase of visual sensitivity at the cued location. Time course, spatial specificity, and magnitude of this improvement, however, were specific to each stimulus. Based on our findings, we present guidelines to select the stimulus best suited to measure visuospatial attention depending on the respective research question.

Oculomotor selection underlies feature retention in visual working memory.

Oculomotor selection, spatial task relevance, and visual working memory (WM) are described as three processes highly intertwined and sustained by similar cortical structures. However, because task-relevant locations always constitute potential saccade targets, no study so far has been able to distinguish between oculomotor selection and spatial task relevance. We designed an experiment that allowed us to dissociate in humans the contribution of task relevance, oculomotor selection, and oculomotor execution to the retention of feature representations in WM. We report that task relevance and oculomotor selection lead to dissociable effects on feature WM maintenance. In a first task, in which an object's location was encoded as a saccade target, its feature representations were successfully maintained in WM, whereas they declined at nonsaccade target locations. Likewise, we observed a similar WM benefit at the target of saccades that were prepared but never executed. In a second task, when an object's location was marked as task relevant but constituted a nonsaccade target (a location to avoid), feature representations maintained at that location did not benefit. Combined, our results demonstrate that oculomotor selection is consistently associated with WM, whereas task relevance is not. This provides evidence for an overlapping circuitry serving saccade target selection and feature-based WM that can be dissociated from processes encoding task-relevant locations.

Presaccadic attention sharpens visual acuity.

Visual perception is limited by spatial resolution, the ability to discriminate fine details. Spatial resolution not only declines with eccentricity but also differs for polar angle locations around the visual field, also known as 'performance fields'. To compensate for poor peripheral resolution, we make rapid eye movements-saccades-to bring peripheral objects into high-acuity foveal vision. Already before saccade onset, visual attention shifts to the saccade target location and prioritizes visual processing. This presaccadic shift of attention improves performance in many visual tasks, but whether it changes resolution is unknown. Here, we investigated whether presaccadic attention sharpens peripheral spatial resolution; and if so, whether such effect interacts with performance fields asymmetries. We measured acuity thresholds in an orientation discrimination task during fixation and saccade preparation around the visual field. The results revealed that presaccadic attention sharpens acuity, which can facilitate a smooth transition from peripheral to foveal representation. This acuity enhancement is similar across the four cardinal locations; thus, the typically robust effect of presaccadic attention does not change polar angle differences in resolution.

Dissociable roles of human frontal eye fields and early visual cortex in presaccadic attention - evidence from TMS.

Shortly before each saccadic eye movement, presaccadic attention improves visual sensitivity at the saccade target 1-5 at the expense of lowered sensitivity at non-target locations 6-11 . Some behavioral and neural correlates of presaccadic attention and covert attention -which likewise enhances sensitivity, but during fixation 12 -are similar 13 . This resemblance has led to the debatable 13-18 notion that presaccadic and covert attention are functionally equivalent and rely on the same neural circuitry 19-21 . At a broad scale, oculomotor brain structures (e.g., FEF) are also modulated during covert attention 22-24 - yet by distinct neuronal subpopulations 25-28 . Perceptual benefits of presaccadic attention rely on feedback from oculomotor structures to visual cortices 29,30 ( Fig. 1a ); micro-stimulation of FEF in non-human primates affects activity in visual cortex 31-34 and enhances visual sensitivity at the movement field of the stimulated neurons 35-37 . Similar feedback projections seem to exist in humans: FEF+ activation precedes occipital activation during saccade preparation 38,39 and FEF TMS modulates activity in visual cortex 40-42 and enhances perceived contrast in the contralateral hemifield 40 . We investigated presaccadic feedback in humans by applying TMS to frontal or visual areas during saccade preparation. By simultaneously measuring perceptual performance, we show the causal and differential roles of these brain regions in contralateral presaccadic benefits at the saccade target and costs at non-targets: Whereas rFEF+ stimulation reduced presaccadic costs throughout saccade preparation, V1/V2 stimulation reduced benefits only shortly before saccade onset. These effects provide causal evidence that presaccadic attention modulates perception through cortico-cortical feedback and further dissociate presaccadic and covert attention.

Dissociable roles of human frontal eye fields and early visual cortex in presaccadic attention.

Shortly before saccadic eye movements, visual sensitivity at the saccade target is enhanced, at the expense of sensitivity elsewhere. Some behavioral and neural correlates of this presaccadic shift of attention resemble those of covert attention, deployed during fixation. Microstimulation in non-human primates has shown that presaccadic attention modulates perception via feedback from oculomotor to visual areas. This mechanism also seems plausible in humans, as both oculomotor and visual areas are active during saccade planning. We investigated this hypothesis by applying TMS to frontal or visual areas during saccade preparation. By simultaneously measuring perceptual performance, we show their causal and differential roles in contralateral presaccadic attention effects: Whereas rFEF+ stimulation enhanced sensitivity opposite the saccade target throughout saccade preparation, V1/V2 stimulation reduced sensitivity at the saccade target only shortly before saccade onset. These findings are consistent with presaccadic attention modulating perception through cortico-cortical feedback and further dissociate presaccadic and covert attention.

The Extrafoveal Preview Effect is More Pronounced at Polar Angle Locations Where Perception is Poor.

The pre-saccadic preview of a peripheral target enhances the efficiency of its post-saccadic processing, termed the extrafoveal preview effect. Peripheral visual performance -and thus the quality of the preview- varies around the visual field, even at iso-eccentric locations. To investigate whether these polar angle asymmetries influence the preview effect, we asked human participants (N=14) to preview four tilted Gabors at the cardinals, until a central cue indicated to which one to saccade. During the saccade, the target orientation either remained or was flipped (valid/invalid preview). After saccade landing, participants discriminated the orientation of the (briefly presented) second Gabor. Gabor contrast was titrated with adaptive staircases. Valid previews increased participants' post-saccadic contrast sensitivity. This preview effect was inversely related to polar angle perceptual asymmetries; largest at the upper, and smallest at the horizontal meridian. Our finding reveals that the visual system compensates for peripheral asymmetries when integrating information across saccades.

EasyEyes - A new method for accurate fixation in online vision testing.

Online methods allow testing of larger, more diverse populations, with much less effort than in-lab testing. However, many psychophysical measurements, including visual crowding, require accurate eye fixation, which is classically achieved by testing only experienced observers who have learned to fixate reliably, or by using a gaze tracker to restrict testing to moments when fixation is accurate. Alas, both approaches are impractical online as online observers tend to be inexperienced, and online gaze tracking, using the built-in webcam, has a low precision (±4 deg). EasyEyes open-source software reliably measures peripheral thresholds online with accurate fixation achieved in a novel way, without gaze tracking. It tells observers to use the cursor to track a moving crosshair. At a random time during successful tracking, a brief target is presented in the periphery. The observer responds by identifying the target. To evaluate EasyEyes fixation accuracy and thresholds, we tested 12 naive observers in three ways in a counterbalanced order: first, in the laboratory, using gaze-contingent stimulus presentation; second, in the laboratory, using EasyEyes while independently monitoring gaze using EyeLink 1000; third, online at home, using EasyEyes. We find that crowding thresholds are consistent and individual differences are conserved. The small root mean square (RMS) fixation error (0.6 deg) during target presentation eliminates the need for gaze tracking. Thus, this method enables fixation-dependent measurements online, for easy testing of larger and more diverse populations.

EasyEyes - Accurate fixation for online vision testing of crowding and beyond.

Online methods allow testing of larger, more diverse populations, with much less effort than in-lab testing. However, many psychophysical measurements, including visual crowding, require accurate eye fixation, which is classically achieved by testing only experienced observers who have learned to fixate reliably, or by using a gaze tracker to restrict testing to moments when fixation is accurate. Alas, both approaches are impractical online since online observers tend to be inexperienced, and online gaze tracking, using the built-in webcam, has a low precision (±4 deg, Papoutsaki et al., 2016). The EasyEyes open-source software reliably measures peripheral thresholds online with accurate fixation achieved in a novel way, without gaze tracking. EasyEyes tells observers to use the cursor to track a moving crosshair. At a random time during successful tracking, a brief target is presented in the periphery. The observer responds by identifying the target. To evaluate EasyEyes fixation accuracy and thresholds, we tested 12 naive observers in three ways in a counterbalanced order: first, in the lab, using gaze-contingent stimulus presentation (Kurzawski et al., 2023; Pelli et al., 2016); second, in the lab, using EasyEyes while independently monitoring gaze; third, online at home, using EasyEyes. We find that crowding thresholds are consistent (no significant differences in mean and variance of thresholds across ways) and individual differences are conserved. The small root mean square (RMS) fixation error (0.6 deg) during target presentation eliminates the need for gaze tracking. Thus, EasyEyes enables fixation-dependent measurements online, for easy testing of larger and more diverse populations.

Presaccadic attention enhances contrast sensitivity, but not at the upper vertical meridian.

Visual performance has striking polar performance asymmetries: At a fixed eccentricity, it is better along the horizontal than vertical meridian and the lower than upper vertical meridian. These asymmetries are not alleviated by covert exogenous or endogenous attention, but have been studied exclusively during eye fixation. However, a major driver of everyday attentional orienting is saccade preparation, during which attention automatically shifts to the future eye fixation. This presaccadic attention shift is considered strong and compulsory, and relies on different neural computations and substrates than covert attention. Thus, we asked: Can presaccadic attention compensate for the ubiquitous performance asymmetries observed during eye fixation? Our data replicate polar performance asymmetries during fixation and document the same asymmetries during saccade preparation. Crucially, however, presaccadic attention enhanced contrast sensitivity at the horizontal and lower vertical meridian, but not at the upper vertical meridian. Thus, instead of attenuating performance asymmetries, presaccadic attention exacerbates them.

To look or not to look: dissociating presaccadic and covert spatial attention.

Attention is a central neural process that enables selective and efficient processing of visual information. Individuals can attend to specific visual information either overtly, by making an eye movement to an object of interest, or covertly, without moving their eyes. We review behavioral, neuropsychological, neurophysiological, and computational evidence of presaccadic attentional modulations that occur while preparing saccadic eye movements, and highlight their differences from those of covert spatial endogenous (voluntary) and exogenous (involuntary) attention. We discuss recent studies and experimental procedures on how these different types of attention impact visual performance, alter appearance, differentially modulate the featural representation of basic visual dimensions (orientation and spatial frequency), engage different neural computations, and recruit partially distinct neural substrates. We conclude that presaccadic attention and covert attention are dissociable.

Post-capture processes contribute to statistical learning of distractor locations in visual search.

People can learn to ignore salient distractors that occur frequently at particular locations, making them interfere less with task performance. This effect has been attributed to learnt suppression of the likely distractor locations at a pre-selective stage of attentional-priority computation. However, rather than distractors at frequent (vs rare) locations being just less likely to capture attention, attention may possibly also be disengaged faster from such distractors - a post-selective contribution to their reduced interference. Eye-movement studies confirm that learnt suppression, evidenced by a reduced rate of oculomotor capture by distractors at frequent locations, is a major factor, whereas the evidence is mixed with regard to a role of rapid disengagement However, methodological choices in these studies limited conclusions as to the contribution of a post-capture effect. Using an adjusted design, here we positively establish the rapid-disengagement effect, while corroborating the oculomotor-capture effect. Moreover, we examine distractor-location learning effects not only for distractors defined in a different visual dimension to the search target, but also for distractors defined within the same dimension, which are known to cause particularly strong interference and probability-cueing effects. Here, we show that both oculomotor-capture and disengagement dynamics contribute to this pattern. Additionally, on distractor-absent trials, the slowed responses to targets at frequent distractor locations-that we observe only in same-, but not different-, dimension conditions-arise pre-selectively, in prolonged latencies of the very first saccade. This supports the idea that learnt suppression is implemented at a different level of priority computation with same-versus different-dimension distractors.

Attention capture outside the oculomotor range.

Neurophysiological studies have demonstrated that attentional orienting is associated with activity in fronto-parietal brain areas that play a pivotal role in oculomotor control, such as the lateral intraparietal cortex (LIP), the frontal eye fields (FEF), and the superior colliculus (SC) (e.g., [1]). Accordingly, based on the influential premotor theory of attention, which posits that even covert shifts of spatial attention in the absence of eye movements are elicited by preceding activation in the oculomotor system [2], it has been claimed that attention can only be allocated to where we can potentially make an eye movement [3]. There are two forms of covert spatial attention: exogenous attention is automatic, stimulus-driven, and transiently deployed in ∼100 ms. Conversely, endogenous attention is voluntary, goal-driven, and deployed in a slower (∼300 ms) and sustained manner [4]. Notably, it has been postulated that only exogenous attention, but not endogenous attention, would be restricted to locations within the so-called oculomotor range that is accessible by saccadic eye movements [5,6]. To test this claim, we used a dissociation approach that allowed us to evaluate exogenous attention shifts to locations within and beyond observers' oculomotor range via their disruptive, attention capturing costs for endogenous attention. We found that salient events equally grab exogenous attention both inside and outside the oculomotor range, demonstrating that exogenous attention can shift to locations not reachable by the eyes.

Visual Perception: Attending beyond the Eyes' Reach.

It has been long debated whether visual attention can shift covertly, decoupled from programming eye movements. Now we know that patients with gaze paralysis show conventional benefits of exogenous (involuntary) attention, confirming that covert attention is not driven by oculomotor programming.