Orienting of attention

Bartlett viewed thinking as a high level skill exhibiting ballistic properties that he called its “point of no return”. This paper explores one aspect of cognition through the use of a simple model task in which human subjects are asked to commit attention to a position in visual space other than fixation. This instruction is executed by orienting a covert (attentional) mechanism that seems sufficiently time locked to external events that its trajectory can be traced across the visual field in terms of momentary changes in the efficiency of detecting stimuli. A comparison of results obtained with alert monkeys, brain injured and normal human subjects shows the relationship of this covert system to saccadic eye movements and to various brain systems controlling perception and motion. In accordance with Bartlett's insight, the possibility is explored that similar principles apply to orienting of attention toward sensory input and orienting to the semantic structures used in thinking.     

Orienting of attention: Then and now

It is nearly 35 years since I gave the 7th Sir Frederick Bartlett lecture at Oxford University. This was published as a paper entitled “Orienting of attention in the quarterly journal”. The topic was then primarily in psychology, but now equally often in neuroscience. This paper summarizes the background of the reaction time methods used in the original paper and findings that emerged later on the sensory consequences of orienting, mainly in the visual system. It then discusses the brain network that is the source of the sensory amplification and other brain networks that are involved in attention. Next, it reviews studies of the development of attentional networks in early life. Finally, it indicates how the new tools available to explore the human brain can lead to further progress.     

Class size,pupil attentiveness and peer relations

Background: Despite a long‐running debate over the effects of class size differences on educational performance there is little evidence on the classroom processes that might be involved. Aims: The effects of class size differences are examined in relation to social and behavioural adjustment to school, in terms of two dimensions: attentiveness and peer relations. It was predicted that as class size increased there would be more inattentiveness in class and more signs of social difficulties between children in the form of more rejection, asocial, anxious and aggressive behaviour, and less prosocial behaviour. Samples: Data came from a large‐scale longitudinal study of children over KS1 (4‐7 years). The observation study was based on a subsample of 235 children in 21 small (average 19 children) and 18 large (average 33 children) reception classes (aged 5 years). The PBR sample involved over 5,000. Methods: There were two complementary methods of data collection: first, a systematic observation study of pre‐selected target children in terms of three ‘social modes’ — when with their teachers, other children and when not interacting — and in terms of work, procedural, social and off‐task activities; and, second, a teacher administered Pupil Behaviour Rating (PBR) scale comprising over 50 items rated on a 3‐point scale grouped into six ‘factors’: hyperactive/distractible, aggressive, anxious/fearful, prosocial, asocial, and excluded. Results: Observations showed that children in large classes were more likely to show off‐task behaviour of all kinds, and more likely to interact with their peers in terms of off‐task behaviour, social, and also on‐task behaviours. Connections between class size and PBR factors were not strong. There was no support for the view that peer relations are better in smaller classes; indeed, there was a slight tendency for worse peer relations, in terms of aggression, asocial and excluded, in the smallest classes. Conclusions: There was confirmation that children in large classes are more distracted from work and more often off task. The unexpected result, based on teacher ratings, that small classes may lead to less social and more aggressive relations between children is discussed, along with implications for teachers of a tendency for more peer‐related contacts in large classes.     

The effects of sound on pupil size and the pupil light reflex

The effects of auditory stimulation on pupil size and the pupil light reflex were investigated in 33 male volunteers. A 95dB tone caused pupillary dilation and a reduction in the amplitude of the light reflex. Although the light reflex amplitude was positively correlated with pupil size in the resting state the effects of noise on the two measures were independent since the pupillary dilation response showed a marked habituation after two presentations of the tone whereas the effect on the light reflex remained the same. People showing high impulsivity scores on the EPQ tended to have smaller pupils (i.e. low arousal). There was also a relationship between impulsivity and light reflex amplitude, but this was probably a secondary consequence of the relationship between the latter measure and pupil size in the resting state.     

Orienting of attention with eye and arrow cues and the effect of overtraining

In contrast to the classical distinction between a controlled orienting of attention induced by central cues and an automatic capture induced by peripheral cues, recent studies suggest that central cues, such as eyes and arrows, may trigger a reflexive-like attentional shift. Yet, it is not clear if the attention shifts induced by these two cues are similar or if they differ in some important aspect. To answer this question, in Experiment 1 we directly compared eye and arrow cues in a counter-predictive paradigm while in Experiment 2 we compared the above cues with a different symbolic cue. Finally, in Experiment 3 we tested the role of over-learned associations in cueing effects. The results provide evidence that eyes and arrows induce identical behavioural effects. Moreover, they show that over-learned associations between spatially neutral symbols and the cued location play an important role in yielding early attentional effects.     

Orienting of attention via observed eye gaze is head-centred

Observing averted eye gaze results in the automatic allocation of attention to the gazed-at location. The role of the orientation of the face that produces the gaze cue was investigated. The eyes in the face could look left or right in a head-centred frame, but the face itself could be oriented 90 degrees clockwise or anticlockwise such that the eyes were gazing up or down. Significant cueing effects to targets presented to the left or right of the screen were found in these head orientation conditions. This suggests that attention was directed to the side to which the eyes would have been looking towards, had the face been presented upright. This finding provides evidence that head orientation can affect gaze following, even when the head orientation alone is not a social cue. It also shows that the mechanism responsible for the allocation of attention following a gaze cue can be influenced by intrinsic object-based (i.e. head-centred) properties of the task-irrelevant cue.     

Orienting attention via observed gaze shift evokes longer term inhibitory effects: implications for social interactions, attention, and memory

One component of successful social interactions is joint attention. It is now well established that when a gaze shift is observed, the observer's attention rapidly and automatically orients to the same location in space. It is also established that such attention shifts via gaze are relatively transient and do not evoke subsequent inhibition processes. In contrast to this conventional view, the authors conducted a series of studies that showed that these properties of gaze attention shift are not necessarily the case in all situations. The article demonstrates (a) gaze cuing over longer intervals than previously observed, (b) that these longer term effects can be inhibitory, and (c) that the longer term gaze cuing effects do not appear to be contingent on retrieval associated with a particular face identity.     

Looking at remembering: Eye movements,pupil size,and autobiographical memory

To examine the relationship between visual imagery and autobiographical memory, eye position and pupil size were recorded while participants first searched for memories and then reconstructed the retrieved memories (Experiment 1), or only searched for memories (Experiment 2). In Experiment 1, we observed that, although recollective experience was not associated with the number of fixations per minute, memories that took longer to retrieve were linked to increased pupil size. In Experiment 2, we observed that directly retrieved memories were recalled more quickly and were accompanied by smaller pupils than generatively retrieved memories. After correcting for response time, retrieval mode also produced an effect, showing that decreased pupil size is not simply due to directly retrieved memories being recalled more quickly. These findings provide compelling evidence that objective measures, such as pupil size, can be used alongside subjective measures, such as self-reports, to distinguish between directly retrieved and generatively retrieved memories.     

Foundations of attention sharing: Orienting and responding to attention in term and preterm 5-month-old infants

Attention is the gateway to perceptual, cognitive, and socioemotional development in humans. We observed 104 5-month-old term and preterm infants and their mothers in social interactions to address three questions about the role of maturation in orienting and responding to attention. We used a fine-grained coding system to allow parallel comparisons across infant and maternal orienting, and sequential analysis to evaluate infant and maternal responding to attention. Orienting and responding to attention differed for attention to people versus objects, as did the relations between maturity and attention. We conclude that maturity contributes to orienting and responding to attention and that orienting and responding to attention are specific rather than homogenous. We discuss the implications of these conclusions for future studies of how attention influences cognitive and communicative development.     

The relationship between baseline pupil size and intelligence

Pupil dilations of the eye are known to correspond to central cognitive processes. However, the relationship between pupil size and individual differences in cognitive ability is not as well studied. A peculiar finding that has cropped up in this research is that those high on cognitive ability have a larger pupil size, even during a passive baseline condition. Yet these findings were incidental and lacked a clear explanation. Therefore, in the present series of studies we systematically investigated whether pupil size during a passive baseline is associated with individual differences in working memory capacity and fluid intelligence. Across three studies we consistently found that baseline pupil size is, in fact, related to cognitive ability. We showed that this relationship could not be explained by differences in mental effort, and that the effect of working memory capacity and fluid intelligence on pupil size persisted even after 23 sessions and taking into account the effect of novelty or familiarity with the environment. We also accounted for potential confounding variables such as; age, ethnicity, and drug substances. Lastly, we found that it is fluid intelligence, more so than working memory capacity, which is related to baseline pupil size. In order to provide an explanation and suggestions for future research, we also consider our findings in the context of the underlying neural mechanisms involved.     

Effect of pupil size on dynamic visual acuity

This study was conducted to assess the effect of pupil size on dynamic visual acuity (DVA). 60 young healthy men (M = 28.1 yr., SD = 3.9) with normal vision were divided into three age-matched groups by pupil size: dilated (n=20), unchanged (n=20), and constricted (n=20). DVA was measured binocularly with freehead viewing before and at 30 min. after each drop was instilled. Each of the three groups got a different amount. The sizes of the constricted, unchanged, and dilated pupils were 2.8 mm (SD = 0.5), 4.1 mm (SD = 0.3), and 7.8 mm (SD = 0.5), respectively. The pupil size x DVA interaction was significant (F(2,114)= 6.07). DVA in the constricted pupil decreased, but that in the dilated pupil increased (paired t test). DVA in the unchanged pupil did not change significantly (paired t test). Pupil size is possibly one of the factors which may affect DVA measurement.     

Mapping and correcting the influence of gaze position on pupil size measurements

Pupil size is correlated with a wide variety of important cognitive variables and is increasingly being used by cognitive scientists. Pupil data can be recorded inexpensively and non-invasively by many commonly used video-based eye-tracking cameras. Despite the relative ease of data collection and increasing prevalence of pupil data in the cognitive literature, researchers often underestimate the methodological challenges associated with controlling for confounds that can result in misinterpretation of their data. One serious confound that is often not properly controlled is pupil foreshortening error (PFE)—the foreshortening of the pupil image as the eye rotates away from the camera. Here we systematically map PFE using an artificial eye model and then apply a geometric model correction. Three artificial eyes with different fixed pupil sizes were used to systematically measure changes in pupil size as a function of gaze position with a desktop EyeLink 1000 tracker. A grid-based map of pupil measurements was recorded with each artificial eye across three experimental layouts of the eye-tracking camera and display. Large, systematic deviations in pupil size were observed across all nine maps. The measured PFE was corrected by a geometric model that expressed the foreshortening of the pupil area as a function of the cosine of the angle between the eye-to-camera axis and the eye-to-stimulus axis. The model reduced the root mean squared error of pupil measurements by 82.5 % when the model parameters were pre-set to the physical layout dimensions, and by 97.5 % when they were optimized to fit the empirical error surface.     

Lateralisation of emotions: evidence from pupil size measurement

The way our brain processes emotional stimuli has been studied intensively. One of the main issues still under debate is the laterality of valence processing. Herein, we employed the fact that pupil size increases under conditions of higher mental effort and during emotional processing, in order to contrast three proposed hypotheses in the field. We used different manual response mapping for emotional stimuli: Participants responded with their right hand for positive and with their left hand for negative facial expressions, or vice versa. The hands position was either regular (Experiment 1) or crossed (Experiment 2) in order to rule out a “spatial-valence association” alternate explanation. A third experiment was conducted by employing a passive viewing procedure of peripheral emotional stimuli. In the first two experiments, pupil size was larger when participants responded to positive stimuli with their left hand and to negative with their right hand, compared with the opposite mapping. Results of Experiment 3 strengthen the findings of Experiments 1 and 2. These findings provide significant psychophysiological evidence for the valence hypothesis: Processing positive stimuli involves the left hemisphere, while processing negative stimuli involves the right hemisphere. These results are discussed in relation to contemporary theories of emotion processing.     

Processing of observed pupil size modulates perception of sadness and predicts empathy

Facial autonomic responses may contribute to emotional communication and reveal individual affective style. In this study, the authors examined how observed pupillary size modulates processing of facial expression, extending the finding that incidentally perceived pupils influence ratings of sadness but not those of happy, angry, or neutral facial expressions. Healthy subjects rated the valence and arousal of photographs depicting facial muscular expressions of sadness, surprise, fear, and disgust. Pupil sizes within the stimuli were experimentally manipulated. Subjects themselves were scored with an empathy questionnaire. Diminishing pupil size linearly enhanced intensity and valence judgments of sad expressions (but not fear, surprise, or disgust). At debriefing, subjects were unaware of differences in pupil size across stimuli. These observations complement an earlier study showing that pupil size directly influences processing of sadness but not other basic emotional facial expressions. Furthermore, across subjects, the degree to which pupil size influenced sadness processing correlated with individual differences in empathy score. Together, these data demonstrate a central role of sadness processing in empathetic emotion and highlight the salience of implicit autonomic signals in affective communication.     

The wide-angle reflection eye camera for visual choice and pupil size

A new equipment has been devised to photograph the reflection of the stimulus scene in the eye. The resulting motion pictures show the pupil encircling the area of the scene which was being fixated by the gaze; they also show the pupil size. Both measurements are simplified by providing a calibrated edge to the scene. No bite bar is required, and the equipment is quick and easy to use, being especially suitable for young children and also for monkeys.