Distractor Evoked Deviations of Saccade Trajectory Are Modulated by Fixation Activity in the Superior Colliculus: Computational and Behavioral Evidence

Previous studies have shown that saccades may deviate towards or away from task irrelevant visual distractors. This observation has been attributed to active suppression (inhibition) of the distractor location unfolding over time: early in time inhibition at the distractor location is incomplete causing deviation towards the distractor, while later in time when inhibition is complete the eyes deviate away from the distractor. In a recent computational study, Wang, Kruijne and Theeuwes proposed an alternative theory that the lateral interactions in the superior colliculus (SC), which are characterized by short-distance excitation and long-distance inhibition, are sufficient for generating both deviations towards and away from distractors. In the present study, we performed a meta-analysis of the literature, ran model simulations and conducted two behavioral experiments to further explore this unconventional theory. Confirming predictions generated by the model simulations, the behavioral experiments show that a) saccades deviate towards close distractors and away from remote distractors, and b) the amount of deviation depends on the strength of fixation activity in the SC, which can be manipulated by turning off the fixation stimulus before or after target onset (Experiment 1), or by varying the eccentricity of the target and distractor (Experiment 2).     

Top-Down but Not Bottom-Up Visual Scanning is Affected in Hereditary Pure Cerebellar Ataxia

The aim of this study was to clarify the nature of visual processing deficits caused by cerebellar disorders. We studied the performance of two types of visual search (top-down visual scanning and bottom-up visual scanning) in 18 patients with pure cerebellar types of spinocerebellar degeneration (SCA6: 11; SCA31: 7). The gaze fixation position was recorded with an eye-tracking device while the subjects performed two visual search tasks in which they looked for a target Landolt figure among distractors. In the serial search task, the target was similar to the distractors and the subject had to search for the target by processing each item with top-down visual scanning. In the pop-out search task, the target and distractor were clearly discernible and the visual salience of the target allowed the subjects to detect it by bottom-up visual scanning. The saliency maps clearly showed that the serial search task required top-down visual attention and the pop-out search task required bottom-up visual attention. In the serial search task, the search time to detect the target was significantly longer in SCA patients than in normal subjects, whereas the search time in the pop-out search task was comparable between the two groups. These findings suggested that SCA patients cannot efficiently scan a target using a top-down attentional process, whereas scanning with a bottom-up attentional process is not affected. In the serial search task, the amplitude of saccades was significantly smaller in SCA patients than in normal subjects. The variability of saccade amplitude (saccadic dysmetria), number of re-fixations, and unstable fixation (nystagmus) were larger in SCA patients than in normal subjects, accounting for a substantial proportion of scattered fixations around the items. Saccadic dysmetria, re-fixation, and nystagmus may play important roles in the impaired top-down visual scanning in SCA, hampering precise visual processing of individual items.     

Asymmetry of the amplitude-temporal properties of visually-guided saccades in monkeys depending on the complexity of the spatial scheme of the visual stimulation

The properties of visually-guided saccades were studied in three monkeys (Macaca rhesus). Traditional single-step GAP-OVERLAP temporal paradigms were used. Target stimuli were presented in accordance with two spatial stimulation schemes: (i) along the horizontal meridian (one-dimensional scheme) and (ii) within rectangle part of the visual field (two-dimensional scheme). We revealed asymmetric focuses of short- and long-latency saccades in the two-dimensional scheme of stimulation. The MANOVA revealed that the factor of dimensionality influenced saccadic latency to a greater extent than the factor of lateralization of stimuli (presenting in the right or left visual hemifields). Accuracy of saccades decreased with increasing in their eccentricity in both spatial schemes of stimulation.     

Distractor inhibition predicts individual differences in the attentional blink

Background

The attentional blink (AB) refers to humans'' impaired ability to detect the second of two targets (T2) in a rapid serial visual presentation (RSVP) stream of distractors if it appears within 200–600 ms of the first target (T1). Here we examined whether humans'' ability to inhibit distractors in the RSVP stream is a key determinant of individual differences in T1 performance and AB magnitude.

Methodology/Principal Findings

We presented subjects with RSVP streams (93.3 ms/item) of letters containing white distractors, a red T1 and a green T2. Subjects'' ability to suppress distractors was assessed by determining the extent to which their second target performance was primed by a preceding distractor that shared the same identity as T2. Individual subjects'' magnitude of T2 priming from this distractor was found to be negatively correlated with their T1 accuracy and positively related to their AB magnitude. In particular, subjects with attenuated ABs showed negative priming (i.e., worse T2 performance when the priming distractor appeared in the RSVP stream compared to when it was absent), whereas those with large ABs displayed positive priming (i.e., better T2 performance when the priming distractor appeared in the RSVP stream compared to when it was absent). Thus, a subject''s ability to suppress distractors, as assessed by T2 priming magnitude, predicted both their T1 performance and AB magnitude.

Conclusions/Significance

These results confirm that distractor suppression plays a key role in RSVP target selection and support the hypothesis that the AB results, at least in part, from a failure of distractor inhibition.     

Parallel Mechanisms for Visual Search in Zebrafish

Parallel visual search mechanisms have been reported previously only in mammals and birds, and not animals lacking an expanded telencephalon such as bees. Here we report the first evidence for parallel visual search in fish using a choice task where the fish had to find a target amongst an increasing number of distractors. Following two-choice discrimination training, zebrafish were presented with the original stimulus within an increasing array of distractor stimuli. We found that zebrafish exhibit no significant change in accuracy and approach latency as the number of distractors increased, providing evidence of parallel processing. This evidence challenges theories of vertebrate neural architecture and the importance of an expanded telencephalon for the evolution of executive function.     

Neuronal correlates of the set-size effect in monkey lateral intraparietal area

It has long been known that the brain is limited in the amount of sensory information that it can process at any given time. A well-known form of capacity limitation in vision is the set-size effect, whereby the time needed to find a target increases in the presence of distractors. The set-size effect implies that inputs from multiple objects interfere with each other, but the loci and mechanisms of this interference are unknown. Here we show that the set-size effect has a neural correlate in competitive visuo-visual interactions in the lateral intraparietal area, an area related to spatial attention and eye movements. Monkeys performed a covert visual search task in which they discriminated the orientation of a visual target surrounded by distractors. Neurons encoded target location, but responses associated with both target and distractors declined as a function of distractor number (set size). Firing rates associated with the target in the receptive field correlated with reaction time both within and across set sizes. The findings suggest that competitive visuo-visual interactions in areas related to spatial attention contribute to capacity limitations in visual searches.     

Latency of visually evoked saccadic eye movements

The paper deals with the initiation of visually guided saccades, in order to break down the saccadic reaction time into functionally different periods of time. It takes into account that spatial processing of information is so basic that modelling of saccadic control properties should include spatio-temporal arrangements. The output signal of the saccadic system was measured in response to visual stimuli in which the time between the appearance of a visual stimulus in the peripheral field and the disappearance of the central fixation point was varied. The variation of the mean saccadic latency time, measured with respect to the onset of the peripheral stimulus, as a function of stimulus asynchrony was highly significant. This variation may be represented by a so-called gap-overlap curve, which is characterized here by means of five parameters. A facilitation model is introduced to fit the results of the gap-overlap experiments. The facilitation model for the initiation of visually evoked saccades incorporates a mechanism which governs the efficiency of processing of signals that arise from a stimulus presented at a particular position in space. It explains how visual information may be affected by other sensory information before it is used to command further saccades. It allows determination of saccadic system parameters, such as the peripheral and the foveal afferent processing time, the central processing time for a saccade and the degree of facilitation. These quantities were found to be characteristic for the given test subjects, and where these data could be compared with neurophysiological data, the agreement was within the experimental error.     

Evidence Inhibition Responds Reactively to the Salience of Distracting Information during Focused Attention

Along with target amplification, distractor inhibition is regarded as a major contributor to selective attention. Some theories suggest that the strength of inhibitory processing is proportional to the salience of the distractor (i.e., inhibition reacts to the distractor intensity). Other theories suggest that the strength of inhibitory processing does not depend on the salience of the distractor (i.e., inhibition does not react to the distractor intensity). The present study aimed to elucidate the relationship between the intensity of a distractor and its subsequent inhibition during focused attention. A flanker task with a variable distractor-target stimulus-onset asynchrony (SOA) was used to measure both distractor interference and distractor inhibition. We manipulated the intensity of the distractor in two separate ways, by varying its distance from the target (Experiment 1) and by varying its brightness (Experiment 2). The results indicate that more intense distractors were associated with both increased interference and stronger distractor inhibition. The latter outcome provides novel support for the reactive inhibition hypothesis, which posits that inhibition reacts to the strength of distractor input, such that more salient distractors elicit stronger inhibition.     

Familiar Face Detection in 180ms

The visual system is tuned for rapid detection of faces, with the fastest choice saccade to a face at 100ms. Familiar faces have a more robust representation than do unfamiliar faces, and are detected faster in the absence of awareness and with reduced attentional resources. Faces of family and close friends become familiar over a protracted period involving learning the unique visual appearance, including a view-invariant representation, as well as person knowledge. We investigated the effect of personal familiarity on the earliest stages of face processing by using a saccadic-choice task to measure how fast familiar face detection can happen. Subjects made correct and reliable saccades to familiar faces when unfamiliar faces were distractors at 180ms—very rapid saccades that are 30 to 70ms earlier than the earliest evoked potential modulated by familiarity. By contrast, accuracy of saccades to unfamiliar faces with familiar faces as distractors did not exceed chance. Saccades to faces with object distractors were even faster (110 to 120 ms) and equivalent for familiar and unfamiliar faces, indicating that familiarity does not affect ultra-rapid saccades. We propose that detectors of diagnostic facial features for familiar faces develop in visual cortices through learning and allow rapid detection that precedes explicit recognition of identity.     

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.     

Slow Cortical Potentials Preceeding Visually Guided Saccades in Schizophrenics

The parameters of saccades and presaccadic slow potentials were studied in right-handed men with a dominant right eye, including 19 schizophrenics and 12 healthy subjects. For visual stimulation, three light-emitting diodes were used, which were located in the center of the visual field (the central fixation stimulus) and 10° to the right and left of it (peripheral stimuli). Two stimulation protocols were used: with a simultaneous switching off of the central fixation stimulus and switching on of the peripheral stimuli (test 1) and with an interstimulus gap of 200 ms (test 2). According to the latency, saccades were divided into anticipatory, express, and regular. Slow EEG potentials preceding regular saccades were analyzed. It was found that the proportion of anticipatory saccades is considerably higher than the normal value in schizophrenia. The analysis of the presaccadic potentials demonstrated a significant decrease in the amplitude of negative potentials in the vertex region at early stages of presaccadic preparation and its increase in the occipital region at late stages. Test 2 in the patients demonstrated an increase in the positivity focus in the frontal region of the right hemisphere. It was assumed that the alterations found in schizophrenia result from the deficit of frontal cortical fields.     

Adults with Dyslexia Demonstrate Large Effects of Crowding and Detrimental Effects of Distractors in a Visual Tilt Discrimination Task

Previous research has shown that adults with dyslexia (AwD) are disproportionately impacted by close spacing of stimuli and increased numbers of distractors in a visual search task compared to controls [1]. Using an orientation discrimination task, the present study extended these findings to show that even in conditions where target search was not required: (i) AwD had detrimental effects of both crowding and increased numbers of distractors; (ii) AwD had more pronounced difficulty with distractor exclusion in the left visual field and (iii) measures of crowding and distractor exclusion correlated significantly with literacy measures. Furthermore, such difficulties were not accounted for by the presence of covarying symptoms of ADHD in the participant groups. These findings provide further evidence to suggest that the ability to exclude distracting stimuli likely contributes to the reported visual attention difficulties in AwD and to the aetiology of literacy difficulties. The pattern of results is consistent with weaker and asymmetric attention in AwD.     

Active maintenance of associative mnemonic signal in monkey inferior temporal cortex

We investigated the contribution of the inferior temporal (IT) cortical neurons to the active maintenance of internal representations. The activity of single neurons in the IT cortex was recorded while the monkeys performed a sequential-type associative memory task in which distractor stimuli interrupted the delay epoch between the cue and target (paired-associate) stimuli. For each neuron, information about each stimulus conveyed by the delay activity was estimated as a coefficient of multiple regression analysis. We found that target information derived from long-term memory (LTM) persisted despite the distractors. By contrast, cue information derived from the visual system was attenuated and frequently replaced by distractor information. These results suggest that LTM-derived information required for upcoming behavior is actively maintained in the IT neurons, whereas visually derived information tends to be updated irrespective of behavioral relevance.     

Saccade latency during probability presentation of the visual targets in man

The latent periods of saccadic eye movements in response to peripheral visual stimuli were measured in 8 right-handed healthy subjects using Posner's paradigm "COST-BENEFIT". In 6 subjects, the saccade latency in response to visual target presented in expected location in valid condition was shorter than that in neutral condition ("benefit"). Increase in saccade latency in response to the visual target presented in unexpected location in valid condition versus neutral condition took place only in 4 subjects ("cost"). A decrease in left-directed saccade latency in response to expected target presented in the left hemifield and increase in saccade latency in response to unexpected left target in comparison with analogous right-directed saccades were observed in valid condition. This phenomenon can be explained by the dominance of the right hemisphere in the processes of spatial orientation and "disengage" of attention.     

Reward-Priming of Location in Visual Search

Existing visual search research has demonstrated that the receipt of reward will be beneficial for subsequent perceptual and attentional processing of features that have characterized targets, but detrimental for processing of features that have characterized irrelevant distractors. Here we report a similar effect of reward on location. Observers completed a visual search task in which they selected a target, ignored a salient distractor, and received random-magnitude reward for correct performance. Results show that when target selection garnered rewarding outcome attention is subsequently a.) primed to return to the target location, and b.) biased away from the location that was occupied by the salient, task-irrelevant distractor. These results suggest that in addition to priming features, reward acts to guide visual search by priming contextual locations of visual stimuli.     

Lateralization of saccadic latency during monocular presentation of stimuli to a leading and non-leading eye

Saccadic latencies were studied in ten healthy subjects. Peripheral targets were presented monocularly to a leading and nonleading eyes in the right and left hemifields. SS (single step) and OVERLAP (200 ms) schemes of visual stimulation were used. Under OVERLAP conditions, the saccadic latency was longer by 30-39 ms and the number of long-latency saccades was higher than under SS conditions, especially in subjects with mixed asymmetry profiles. In the majority of subjects with right asymmetry profile, the latencies of saccades during stimulation of the leading eye were by 12 ms shorter than during stimulation of the nonleading eye, and the latencies of right saccades were by 24 ms shorter than that of the left saccades independently of the stimulated eye. The obtained results explain some characteristic features of hemyspheric asymmetry in organization of saccadic movements.     

Unintentional Activation of Translation Equivalents in Bilinguals Leads to Attention Capture in a Cross-Modal Visual Task

Using a variant of the visual world eye tracking paradigm, we examined if language non- selective activation of translation equivalents leads to attention capture and distraction in a visual task in bilinguals. High and low proficient Hindi-English speaking bilinguals were instructed to programme a saccade towards a line drawing which changed colour among other distractor objects. A spoken word, irrelevant to the main task, was presented before the colour change. On critical trials, one of the line drawings was a phonologically related word of the translation equivalent of the spoken word. Results showed that saccade latency was significantly higher towards the target in the presence of this cross-linguistic translation competitor compared to when the display contained completely unrelated objects. Participants were also slower when the display contained the referent of the spoken word among the distractors. However, the bilingual groups did not differ with regard to the interference effect observed. These findings suggest that spoken words activates translation equivalent which bias attention leading to interference in goal directed action in the visual domain.     

Latency of visually evoked saccadic eye movements

The validness of a model describing the relation between mean saccadic latency and stimulus asynchrony based on facilitation instead of suppression was tested experimentally. As a result, suppression of signals generated by the onset of a peripheral stimulus due to fixation of another target, giving rise to an increase of mean saccadic latency, does not seem very likely. The influence of the intensity of the fixation target on the latency of visually evoked saccades was studied. According to the facilitation model, the offset of the fixation target induces after an afferent delay, a transition of the state of the facilitation mechanism from the unfacilitated condition into a mode of maximal facilitation. The time-period during which this change is accomplished is called Facilitation-Rise-Time (FRT). An interpretation within the context of the facilitation model of gap-overlap latency data for different values of the intensity of the fixation stimulus suggests, in combination with computer-computations of the model, that lowering of this intensity causes an increase in FRT. The results in normal subjects of step stimulus experiments with a dim fixation point substantiate the hypothesis of a facilitation mechanism, which is triggerable not only by an external signal such as the offset of the fixation point, but also by some internal stimulus independent signal. Moreover, data for tracking by an amblyopic eye seem to support this conclusion. The findings of increased saccadic latencies in amblyopic and Optic Neuritis (ON) eyes suggest a slowing of processing of visual information in the sensory pathways from the central retina, subsequently utilized by the oculomotor system in the generation of saccades.(ABSTRACT TRUNCATED AT 250 WORDS)     

Sequences of predictive eye movements form a fractional Brownian series – implications for self-organized criticality in the oculomotor system

When human subjects are presented with a pair of visual targets that alternate periodically, they track the targets with rapid eye movements known as saccades. In previous work we demonstrated that at low pacing rates (<0.5 Hz), saccades have a latency of about 180 ms, and the latencies are uncorrelated from trial to trial. At high pacing rates (>0.6 Hz), latencies are much shorter: subjects make predictive saccades that anticipate target motion. The predictive latencies are correlated and appear to form a fractional Brownian motion. Here we confirm this finding by examining the rate of decay of nonlinear forecasting of predictive latencies. We further characterize the nature of predictive saccade latencies through the use of detrended fluctuation analysis and surrogate data. These results lead us to conclude that predictive saccades may exhibit a form of self-organized criticality, which enables rapid response to changes in stimulus timing. We provide an experimental demonstration of this.     

Potential of the human cerebral cortex prior to antisaccades

Latencies and other parameters of presaccadic potentials preceding antisaccades and normal saccades to visual stimuli were studied in 10 right-handed healthy subjects. The EEG was recorded in F3, F4, Fz, C3, C4, Cz, P3, P4, O1 and O2 derivation. EEG records preceding saccades and antisaccades with mean latencies were selected and averaged. The latencies of the leftward antisaccades were shorter than of the rightward antisaccades. The slow presaccadic negativity (in the period of central eye fixations) and fast N -2 and P -1 potentials within the latent period were more prominent before antisaccades than normal saccades. Spatiotemporal analyses of presaccadic potentials showed that the right frontal cortex was activated to a greater extent before antisaccades than before saccades. These findings suggest that right-hemispheric dominance in the spatial attention and inhibition of automatic saccades to visual stimuli in the period of antisaccades preparation.