Inhibition of saccadic eye movements to locations in spatial working memory

Inhibition of return (IOR) refers to a bias against overt and covert attentional orienting toward previously attended locations. According to the reorienting hypothesis, IOR is generated when attention is withdrawn from the attended location and is prevented from “returning” to it. The present study investigated whether maintenance of attention at the cued location could affect the inhibition of oculomotor orienting to it. To preclude disengagement of attention, we asked participants to maintain the cued location in working memory. Maintenance of visuospatial information in memory has been shown to be accomplished through a sustained shift of spatial attention to a memorized location. Our results show that oculomotor IOR occurs at a particular location even when that location is kept in working memory (Experiment 1). Furthermore, we demonstrate that the mere act of maintenance of a location in working memory produces oculomotor inhibition similar to IOR (Experiments 2 and 3). We conclude that the oculomotor system is used for coding and maintaining locations in spatial working memory. In addition, we demonstrate that endogenous attention associated with maintenance of a location in working memory can be dissociated from the attention needed for execution of a saccadic eye movement.     

Moving eyes and moving thought: On the spatial compatibility between eye movements and cognition

Grant and Spivey (2003) proposed that eye movement trajectories can influence spatial reasoning by way of an implicit eye-movement-to-cognition link. We tested this proposal and investigated the nature of this link by continuously monitoring eye movements and asking participants to perform a problem-solving task under free-viewing conditions while occasionally guiding their eye movements (via an unrelated tracking task), either in a pattern related to the problem’s solution or in unrelated patterns. Although participants reported that they were not aware of any relationship between the tracking task and the problem, those who moved their eyes in a pattern related to the problem’s solution were the most successful problem solvers. Our results support the existence of an implicit compatibility between spatial cognition and the eye movement patterns that people use to examine a scene.     

Inferences about predictable events: eye movements during reading

 Eye fixations were recorded to assess whether, how, and when readers draw inferences about predictable events. Predicting context sentences, or non-predicting control sentences, were presented, followed by continuation sentences in which a target word referred to a predictable event (inferential word) or an unlikely event (non-predictable word). There were no effects on initial target word processing measures, such as launch and landing sites, fixation probability, first-fixation duration, or first-pass reading time. However, relative to the control condition, the predicting context (1) speeded up reanalysis of the inferential word, as revealed by a reduction in second-pass reading time and regressions, and (2) interfered with processing of the non-predictable word, as shown by an increase in regressions. These results indicate that predictive inferences are active at late text integration processes, rather than at early lexical-access processes. The pattern of findings suggests that these inferences involve initial activation of rather general concepts following the inducing context, and that they are completed or refined with delay, after the inferential target word is read. Received: 4 January 2000 / Accepted: 23 October 2000     

Oculocentric coding of inhibited eye movements to recently attended locations

Results are reported for experiments that examined eye movements directed toward recently cued objects. In 1 experiment participants were slower to initiate saccades toward the earlier location of an object that had been cued, even though the cued object had subsequently moved away from that location. Other experiments involved exploring the reference frame within which the inhibited eye movements are encoded. These experiments revealed that the eye movement that is inhibited is encoded in an oculocentric-rather than an environmental-reference frame. However, simple detection as indexed by manual keypress responses is encoded in an environmental reference frame. The results have implications for inhibition of return, for the link between eye movements and attention, and for the nature of the spatial reference frames in which both covert and overt movements of attention are encoded.     

The relationship between eye movements and spatial attention

Most previous studies of the attentional consequences of making saccadic eye movements have used peripheral stimuli to elicit eye movements. It is argued that in the light of evidence showing automatic “capture” of attention by peripheral stimuli, these experiments do not distinguish between attentional effects due to peripheral stimuli and those due to eye movements. In the present study, spatial attention was manipulated by varying the probability that peripheral probe stimuli would appear in different positions, while saccades were directed by a central arrow, enabling the effects of attention and eye movements to be separated. The results showed that the time to react to a peripheral stimulus could be shortened both by advance knowledge of its likely position and, separately, by preparing to make a saccade to that position. When the saccade was directed away from the most likely position of the probe, the targets for attention and eye movements were on opposite sides of the display. In this condition, the effects of preparing to make a saccade proved to be stronger than the effects of attentional allocation until well after the saccade had finished, suggesting that making a saccade necessarily involves the allocation of attention to the target position. The effects of probe stimuli on saccade latencies were also examined: probe stimuli that appeared before the saccade shortened saccade latencies if they appeared at the saccade target, and lengthened saccade latencies if they appeared on the opposite side of fixation. These facilitatory and inhibitory effects were shown to occur at different stages of saccade preparation and suggest that attention plays an important role in the generation of voluntary eye movements. The results of this study indicate that while it is possible to make attention movements without making corresponding eye movements, it is not possible to make an eye movement (in the absence of peripheral stimulation) without making a corresponding shift in the focus of attention.     

Eye-hand coordination: spatial localization after saccadic and pursuit eye movements

Subjects produced speeded and unspeeded hand movements to a target location after either saccadic or pursuit eye movements to the target. Hand movements began either aligned with the initial position of gaze or from some other location. Subjects generally underestimated the extent of the pursuit eye movements relative to estimates made after saccades. With speeded hand movements, however, the underestimation was reduced considerably if the hand movements began aligned with a location other than the initial position of gaze. The results reveal details of the mechanisms underlying eye-hand coordination and show that important differences exist in the information used for localization for slow and rapid limb movements.     

Search asymmetry and eye movements in infants and adults

Search asymmetry is characterized by the detection of a feature-present target amidst feature-absent distractors being efficient and unaffected by the number of distractors, whereas detection of a feature-absent target amidst feature-present distractors is typically inefficient and affected by the number of distractors. Although studies have attempted to investigate this phenomenon with infants (e.g., Adler, Inslicht, Rovee-Collier, & Gerhardstein in Infant Behavioral Development, 21, 253–272, 1998; Colombo, Mitchell, Coldren, & Atwater in Journal of Experimental Psychology: Learning, Memory and Cognition, 19, 98–109, 1990), due to methodological limitations, their findings have been unable to definitively establish the development of visual search mechanisms in infants. The present study assessed eye movements as a means to examine an asymmetry in responding to feature-present versus feature-absent targets in 3-month-olds, relative to adults. Saccade latencies to localize a target (or a distractor, as in the homogeneous conditions) were measured as infants and adults randomly viewed feature-present (R among Ps), feature-absent (P among Rs), and homogeneous (either all Rs or all Ps) arrays at set sizes of 1, 3, 5, and 8. Results indicated that neither infants’ nor adults’ saccade latencies to localize the target in the feature-present arrays were affected by increasing set sizes, suggesting that localization of the target was efficient. In contrast, saccade latencies to localize the target in the feature-absent arrays increased with increasing set sizes for both infants and adults, suggesting an inefficient localization. These findings indicate that infants exhibit an asymmetry consistent with that found with adults, providing support for functional bottom-up selective attention mechanisms in early infancy.     

Coordinated control of eye and hand movements in dynamic reaching

In the present study, we integrated two recent, at first sight contradictory findings regarding the question whether saccadic eye movements can be generated to a newly presented target during an ongoing hand movement. Saccades were measured during so-called adaptive and sustained pointing conditions. In the adapted pointing condition, subjects had to direct both their gaze and arm movements to a displaced target location. The results showed that the eyes could fixate the new target during pointing. In addition, a temporal coupling of these corrective saccades was found with changes in arm movement trajectories when reaching to the new target. In the sustained pointing condition, however, the same subjects had to point to the initial target, while trying to deviate their gaze to a new target that appeared during pointing. It was found that the eyes could not fixate the new target before the hand reached the initial target location. Together, the results indicate that ocular gaze is always forced to follow the target intended by a manual arm movement. A neural mechanism is proposed that couples ocular gaze to the target of an arm movement. Specifically, the mechanism includes a reach neuron layer besides the well-known saccadic layer in the primate superior colliculus. Such a tight, sub-cortical coupling of ocular gaze to the target of a reaching movement can explain the contrasting behavior of the eyes in dependency of whether the eye and hand share the same target position or attempt to move to different locations.     

Eye movements during language-mediated visual search reveal a strong link between overt visual attention and lexical processing in 36-month-olds

The nature of children’s early lexical processing was investigated by asking what information 36-month-olds access and use when instructed to find a known but absent referent. Children readily retrieved stored knowledge about characteristic color, i.e., when asked to find an object with a typical color (e.g., strawberry), children tended to fixate more upon an object that had the same (e.g., red plane) as opposed to a different (e.g., yellow plane) color. They did so regardless of the fact that they had plenty of time to recognize the pictures for what they are, i.e., planes and not strawberries. These data represent the first demonstration that language-mediated shifts of overt attention in young children can be driven by individual stored visual attributes of known words that mismatch on most other dimensions. The finding suggests that lexical processing and overt attention are strongly linked from an early age.     

The selective disruption of spatial working memory by eye movements

In the late 1970s/early 1980s, Baddeley and colleagues conducted a series of experiments investigating the role of eye movements in visual working memory. Although only described briefly in a book (Baddeley, 1986), these studies have influenced a remarkable number of empirical and theoretical developments in fields ranging from experimental psychology to human neuropsychology to nonhuman primate electrophysiology. This paper presents, in full detail, three critical studies from this series, together with a recently performed study that includes a level of eye movement measurement and control that was not available for the older studies. Together, the results demonstrate several facts about the sensitivity of visuospatial working memory to eye movements. First, it is eye movement control, not movement per se, that produces the disruptive effects. Second, these effects are limited to working memory for locations and do not generalize to visual working memory for shapes. Third, they can be isolated to the storage/maintenance components of working memory (e.g., to the delay period of the delayed-recognition task). These facts have important implications for models of visual working memory.     

The selective disruption of spatial working memory by eye movements

In the late 1970s/early 1980s, Baddeley and colleagues conducted a series of experiments investigating the role of eye movements in visual working memory. Although only described briefly in a book (Baddeley, 1986 Baddeley AD 1986 Working memory London Oxford University Press  [Google Scholar]), these studies have influenced a remarkable number of empirical and theoretical developments in fields ranging from experimental psychology to human neuropsychology to nonhuman primate electrophysiology. This paper presents, in full detail, three critical studies from this series, together with a recently performed study that includes a level of eye movement measurement and control that was not available for the older studies. Together, the results demonstrate several facts about the sensitivity of visuospatial working memory to eye movements. First, it is eye movement control, not movement per se, that produces the disruptive effects. Second, these effects are limited to working memory for locations and do not generalize to visual working memory for shapes. Third, they can be isolated to the storage/maintenance components of working memory (e.g., to the delay period of the delayed-recognition task). These facts have important implications for models of visual working memory.     

The effect of spatial frequency content on parameters of eye movements

Two experiments were conducted to examine the influence of the spatial frequency content of natural images on saccadic size and fixation duration. In the first experiment 10 pictures of natural textures were low-pass filtered (0.04-0.76 cycles/deg) and high-pass filtered (1.91-19.56 cycles/deg) and presented with the unfiltered originals in random order, each for 10 s, to 18 participants, with the instruction to inspect them in order to find a suitable name. The participants' eye movements were recorded. It was found that low-pass filtered images resulted in larger saccadic amplitudes compared with high-pass filtered images. A second experiment was conducted with natural stimuli selected for different power spectra which supported the results outlined above. In general, low-spatial frequencies elicit larger saccades associated with shorter fixation durations whereas high-spatial frequencies elicit smaller saccades with longer fixation durations.     

Effects of context on eye movements when reading about possible and impossible events

Plausibility violations resulting in impossible scenarios lead to earlier and longer lasting eye movement disruption than violations resulting in highly unlikely scenarios (K. Rayner, T. Warren, B. J. Juhasz, & S. P. Liversedge, 2004; T. Warren & K. McConnell, 2007). This could reflect either differences in the timing of availability of different kinds of information (e.g., selectional restrictions, world knowledge, and context) or differences in their relative power to guide semantic interpretation. The authors investigated eye movements to possible and impossible events in real-world and fantasy contexts to determine when contextual information influences detection of impossibility cued by a semantic mismatch between a verb and an argument. Gaze durations on a target word were longer to impossible events independent of context. However, a measure of the time elapsed from first fixating the target word to moving past it showed disruption only in the real-world context. These results suggest that contextual information did not eliminate initial disruption but moderated it quickly thereafter.     

Effects of saccadic bilateral eye movements on memory in children and adults: an exploratory study

The effects of saccadic bilateral (horizontal) eye movements on true and false memory in adults and children were investigated. Both adults and children encoded lists of associated words in the Deese-Roediger-McDermott paradigm followed by a test of recognition memory. Just prior to retrieval, participants were asked to engage in 30s of bilateral vs. vertical vs. no eye movements. For studied information, the results for adults replicated previous work; bilateral eye movements were demonstrated to increase the accuracy of memory by increasing the hit rate and reducing the false alarm rate for related and unrelated recognition test lures. The results for children also indicated an improvement in memory accuracy, and like adults, was due to both an increase in the hit rate and a reduction in the false alarm rate. In spite of these similarities, the effects of bilateral eye movements differed between adults and children for critical unstudied words; i.e., those associated with the theme of the list. Only in adults did, bilateral eye movements reduce associative false memories; children did not show a reduction in false memory for critical associates. This produced a dissociation between the effects of eye movements on associative false memory as a function of age. The results are discussed from a developmental perspective in terms of potential mechanisms underlying true and false memory.     

Adding odor: Less distress and enhanced attention for 6-month-olds

The effect of odor on cognitive and emotional processes has been studied in adults and children, but less so in infants. In this study twenty-seven six-month-olds were presented with a video while in either an odor (pine or baby-powder) or a no odor control condition. The video was a 92-s audiovisual presentation of a woman expressing happiness and sadness, with the order of emotion counterbalanced. Infant attention (looking time) and emotional expression (smiling, crying, mouthing) were coded. Infants looked longer in the presence of odor and expressed less crying and mouthing but more smiling behavior. Presence of odor markedly reduced infant emotional distress and increased attention, suggesting that the olfactory sensory system provides cues to infants that support mood regulation and maintain attention. These results have implications for optimizing infant environments for emotional health and cognitive development.     

Temporal binding of auditory spatial information across dynamic binaural events

Simultaneity judgments were used to measure temporal binding windows (TBW) for brief binaural events (changes in interaural time and/or level differences [ITD and ILD]) and test the hypothesis that ITD and ILD contribute to perception via separate sensory dimensions subject to binding via slow (100+ ms)—presumably cortical—mechanisms as in multisensory TBW. Stimuli were continuous low-frequency noises that included two brief shifts of either type (ITD or ILD), both of which are heard as lateral position changes. TBW for judgments within a single cue dimension were narrower for ITD (mean = 444 ms) than ILD (807 ms). TBW for judgments across cue dimensions (i.e., one ITD shift and one ILD shift) were similar to within-cue ILD (778 ms). The results contradict the original hypothesis, in that cross-cue comparisons were no slower than within-cue ILD comparisons. Rather, the wide TBW values—consistent with previous estimates of multisensory TBW—suggest slow integrative processing for both types of judgments. Narrower TBW for ITD than ILD judgments suggests important cue-specific differences in the neural mechanisms or the perceptual correlates of integration across binaural-cue dimensions.     

Task effects reveal cognitive flexibility responding to frequency and predictability: Evidence from eye movements in reading and proofreading

It is well-known that word frequency and predictability affect processing time. These effects change magnitude across tasks, but studies testing this use tasks with different response types (e.g., lexical decision, naming, and fixation time during reading; Schilling, Rayner, & Chumbley, 1998), preventing direct comparison. Recently, Kaakinen and Hyönä (2010) overcame this problem, comparing fixation times in reading for comprehension and proofreading, showing that the frequency effect was larger in proofreading than in reading. This result could be explained by readers exhibiting substantial cognitive flexibility, and qualitatively changing how they process words in the proofreading task in a way that magnifies effects of word frequency. Alternatively, readers may not change word processing so dramatically, and instead may perform more careful identification generally, increasing the magnitude of many word processing effects (e.g., both frequency and predictability). We tested these possibilities with two experiments: subjects read for comprehension and then proofread for spelling errors (letter transpositions) that produce nonwords (e.g., trcak for track as in Kaakinen & Hyönä) or that produce real but unintended words (e.g., trial for trail) to compare how the task changes these effects. Replicating Kaakinen and Hyönä, frequency effects increased during proofreading. However, predictability effects only increased when integration with the sentence context was necessary to detect errors (i.e., when spelling errors produced words that were inappropriate in the sentence; trial for trail). The results suggest that readers adopt sophisticated word processing strategies to accommodate task demands.