Differential influence of attention on gaze and head movements

A salient peripheral cue can capture attention, influencing subsequent responses to a target. Attentional cueing effects have been studied for head-restrained saccades; however, under natural conditions, the head contributes to gaze shifts. We asked whether attention influences head movements in combined eye-head gaze shifts and, if so, whether this influence is different for the eye and head components. Subjects made combined eye-head gaze shifts to horizontal visual targets. Prior to target onset, a behaviorally irrelevant cue was flashed at the same (congruent) or opposite (incongruent) location at various stimulus-onset asynchrony (SOA) times. We measured eye and head movements and neck muscle electromyographic signals. Reaction times for the eye and head were highly correlated; both showed significantly shorter latencies (attentional facilitation) for congruent compared with incongruent cues at the two shortest SOAs and the opposite pattern (inhibition of return) at the longer SOAs, consistent with attentional modulation of a common eye-head gaze drive. Interestingly, we also found that the head latency relative to saccade onset was significantly shorter for congruent than that for incongruent cues. This suggests an effect of attention on the head separate from that on the eyes.     

The effects of illusory line motion on incongruent saccades: implications for saccadic eye movements and visual attention

A complex neural problem must be solved before a voluntary eye movement is triggered away from a stimulus (antisaccade). The location code activated by a stimulus must be internally translated into an appropriate signal to direct the eyes into the opposite visual field, while the reflexive tendency to look directly at the stimulus must be suppressed. No doubt these extra processes contribute to the ubiquitous slowing of antisaccades. However, there is no consensus on the cognitive mechanisms that contribute to the antisaccade programme. Visual attention is closely associated with the generation of saccadic eye movements and it has been shown that attention will track an illusion of line motion. A series of experiments combined this illusion with a saccadic eye movement that was congruent (i.e. directed towards), or incongruent with (i.e. direct away from), a peripheral target. Experiment 1 showed that congruent saccades had faster reaction times than incongruent saccades. In contrast, Experiments 2 and 3 demonstrated that, with illusory line motion, incongruent saccades now had faster reaction times than congruent saccades. These findings demonstrate that an illusory phenomenon can accelerate the processing of an incongruent relative to a congruent saccade.     

Is gaze following purely reflexive or goal-directed instead? Revisiting the automaticity of orienting attention by gaze cues

Distracting gaze has been shown to elicit automatic gaze following. However, it is still debated whether the effects of perceived gaze are a simple automatic spatial orienting response or are instead sensitive to the context (i.e. goals and task demands). In three experiments, we investigated the conditions under which gaze following occurs. Participants were instructed to saccade towards one of two lateral targets. A face distracter, always present in the background, could gaze towards: (a) a task-relevant target––(“matching” goal-directed gaze shift)––congruent or incongruent with the instructed direction, (b) a task-irrelevant target, orthogonal to the one instructed (“non-matching” goal-directed gaze shift), or (c) an empty spatial location (no-goal-directed gaze shift). Eye movement recordings showed faster saccadic latencies in correct trials in congruent conditions especially when the distracting gaze shift occurred before the instruction to make a saccade. Interestingly, while participants made a higher proportion of gaze-following errors (i.e. errors in the direction of the distracting gaze) in the incongruent conditions when the distracter’s gaze shift preceded the instruction onset indicating an automatic gaze following, they never followed the distracting gaze when it was directed towards an empty location or a stimulus that was never the target. Taken together, these findings suggest that gaze following is likely to be a product of both automatic and goal-driven orienting mechanisms.     

Effects of short-term adaptation of saccadic gaze amplitude on hand-pointing movements

 We investigated whether and how adaptive changes in saccadic amplitudes (short-term saccadic adaptation) modify hand movements when subjects are involved in a pointing task to visual targets without vision of the hand. An experiment consisted of the pre-adaptation test of hand pointing (placing the finger tip on a LED position), a period of adaptation, and a post-adaptation test of hand pointing. In a basic task (transfer paradigm A), the pre- and post-adaptation trials were performed without accompanying eye and head movements: in the double-step gaze adaptation task, subjects had to fixate a single, suddenly displaced visual target by moving eyes and head in a natural way. Two experimental sessions were run with the visual target jumping during the saccades, either backwards (from 30 to 20°, gaze saccade shortening) or onwards (30 to 40°, gaze saccade lengthening). Following gaze-shortening adaptation (level of adaptation 79±10%, mean and s.d.), we found a statistically significant shift (t-test, error level P<0.05) in the final hand-movement points, possibly due to adaptation transfer, representing 15.2% of the respective gaze adaptation. After gaze-lengthening adaptation (level of adaptation 92±17%), a non-significant shift occurred in the opposite direction to that expected from adaptation transfer. The applied computations were also performed on some data of an earlier transfer paradigm (B, three target displacements at a time) with gain shortening. They revealed a significant transfer relative to the amount of adaptation of 18.5±17.5% (P<0.05). In the coupling paradigm (C), we studied the influence of gaze saccade adaptation of hand-pointing movements with concomitant orienting gaze shifts. The adaptation levels achieved were 59±20% (shortening) and 61±27% (lengthening). Shifts in the final fingertip positions were congruent with internal coupling between gaze and hand, representing 53% of the respective gaze-amplitude changes in the shortening session and 6% in the lengthening session. With an adaptation transfer of less than 20% (paradigm A and B), we concluded that saccadic adaptation does not ”automatically” produce a functionally meaningful change in the skeleto-motor system controlling hand-pointing movements. In tasks with concomitant gaze saccades (coupling paradigm C), the modification of hand pointing by the adapted gaze comes out more clearly, but only in the shortening session. Received: 9 February 1998 / Accepted: 18 August 1998     

Developmental differences in cognitive control of socio-affective processing

We examined developmental differences in cognitive control in the context of distracting communicative cues varying in socio-affective significance. Adults and children (6-13 years) performed a Stroop-type task that required manual responses to a target word (LEFT/RIGHT) in the context of to-be-ignored spatial cues that were symbolic (arrow pointing left or right), social (left/right averted eye gaze in faces), or socio-emotional (happy, angry and fearful faces with left/right averted eye gaze). On the basis of the finding that accuracy was lower in the context of spatially incongruent than congruent cues, it was concluded that spatial direction, cued by both arrows and eye gaze, interfered with response selection. Interference did not differ between adults and children indicating that cognitive control of spatial attention directed by symbolic and social information is mature by 6 years. Interference from averted eye gaze was insensitive to the valence of facial emotion in adults and in children between 6-9 but not 10-13 years. Older children showed more interference from averted eye gaze in angry faces than younger children or adults. Thus, cognitive control of socio-affective processing differs in the preadolescent years relative to earlier in late childhood and adulthood.     

Developmental Differences in Cognitive Control of Socio-Affective Processing

We examined developmental differences in cognitive control in the context of distracting communicative cues varying in socio-affective significance. Adults and children (6–13 years) performed a Stroop-type task that required manual responses to a target word (LEFT/RIGHT) in the context of to-be-ignored spatial cues that were symbolic (arrow pointing left or right), social (left/right averted eye gaze in faces), or socio-emotional (happy, angry and fearful faces with left/right averted eye gaze). On the basis of the finding that accuracy was lower in the context of spatially incongruent than congruent cues, it was concluded that spatial direction, cued by both arrows and eye gaze, interfered with response selection. Interference did not differ between adults and children indicating that cognitive control of spatial attention directed by symbolic and social information is mature by 6 years. Interference from averted eye gaze was insensitive to the valence of facial emotion in adults and in children between 6–9 but not 10–13 years. Older children showed more interference from averted eye gaze in angry faces than younger children or adults. Thus, cognitive control of socio-affective processing differs in the preadolescent years relative to earlier in late childhood and adulthood.     

Attentional shift by gaze is triggered without awareness

Reflexive attentional shift in response to another individual’s gaze direction has been reported, but it remains unknown whether this process can occur subliminally. We investigated this issue using facial stimuli consisting of drawings (Experiment 1) and photographs (Experiment 2). The gaze direction was expressed by the eye gaze direction (Experiment 1), and the eye gaze and head direction (Experiment 2). The gaze cue was presented either supraliminally or subliminally in the center of the visual field, before target presentation in the periphery. The task for participants was to localize the target as soon as possible. The reaction time needed to localize the target was consistently shorter for valid than invalid gaze cues for both types of gaze cues in both subliminal and supraliminal conditions. These findings indicate that attentional shift can be triggered even without awareness in response to another individual’s eye gaze or head direction.     

Eye movements affirm: automatic overt gaze and arrow cueing for typical adults and adults with autism spectrum disorder

People with autism spectrum disorder (ASD) show reduced interest towards social aspects of the environment and a lesser tendency to follow other people’s gaze in the real world. However, most studies have shown that people with ASD do respond to eye-gaze cues in experimental paradigms, though it is possible that this behaviour is based on an atypical strategy. We tested this possibility in adults with ASD using a cueing task combined with eye-movement recording. Both eye gaze and arrow pointing distractors resulted in overt cueing effects, both in terms of increased saccadic reaction times, and in proportions of saccades executed to the cued direction instead of to the target, for both participant groups. Our results confirm previous reports that eye gaze cues as well as arrow cues result in automatic orienting of overt attention. Moreover, since there were no group differences between arrow and eye gaze cues, we conclude that overt attentional orienting in ASD, at least in response to centrally presented schematic directional distractors, is typical.     

Verbal instructions and top-down saccade control

Few studies have addressed the interaction between instruction content and saccadic eye movement control. To assess the impact of instructions on top-down control, we instructed 20 healthy volunteers to deliberately delay saccade triggering, to make inaccurate saccades or to redirect saccades—i.e. to glimpse towards and then immediately opposite to the target. Regular pro- and antisaccade tasks were used for comparison. Bottom-up visual input remained unchanged and was a gap paradigm for all instructions. In the inaccuracy and delay tasks, both latencies and accuracies were detrimentally impaired by either type of instruction and the variability of latency and accuracy was increased. The intersaccadic interval (ISI) required to correct erroneous antisaccades was shorter than the ISI for instructed direction changes in the redirection task. The word-by-word instruction content interferes with top-down saccade control. Top-down control is a time consuming process, which may override bottom-up processing only during a limited time period. It is questionable whether parallel processing is possible in top-down control, since the long ISI for instructed direction changes suggests sequential planning.     

Attentional shifts by gaze direction in voluntary orienting: evidence from a microsaccade study

Shifts in spatial attention can be induced by the gaze direction of another. However, it is unclear whether gaze direction influences the allocation of attention by reflexive or voluntary orienting. The present study was designed to examine which type of attentional orienting is elicited by gaze direction. We conducted two experiments to answer this question. In Experiment 1, we used a modified Posner paradigm with gaze cues and measured microsaccades to index the allocation of attention. We found that microsaccade direction followed cue direction between 200 and 400 ms after gaze cues were presented. This is consistent with the latencies observed in other microsaccade studies in which voluntary orienting is manipulated, suggesting that gaze direction elicits voluntary orienting. However, Experiment 1 did not separate voluntary and reflexive orienting directionally, so in Experiment 2, we used an anticue task in which cue direction (direction to allocate attention) was the opposite of gaze direction (direction of gaze in depicted face). The results in Experiment 2 were consistent with those from Experiment 1. Microsaccade direction followed the cue direction, not gaze direction. Taken together, these results indicate that the shift in spatial attention elicited by gaze direction is voluntary orienting.     

Effects of procues on error rate and reaction times of antisaccades in human subjects

In a gap paradigm, where the saccadic reaction times are usually short, the number of express saccades can be further increased and their latency decreased when a valid transient peripheral cue is given 100 ms before target occurrence. In the present study we measured the saccadic reaction times of seven human subjects who had been instructed to make antisaccades (saccades to the side opposite to stimulus presentation) in the gap paradigm. In the first experiment, we presented a 100% valid cue with 100 ms cue lead time. To explore whether the cue reduced the reaction times of the antisaccades, the cue was always presented on the opposite side to where the stimulus occurred (stimulus direction was randomized between 4° to the left and right), and it was thus indicated in each trial to which side the antisaccade was required (procue). In the second set of experiments the cue was consistently presented on either the left or the right side in two different blocks; it was thus noninformative with respect to the direction of the antisaccade. In the first experiment, a significant increase in mean reaction times of correct antisaccades and a considerable increase in erratic prosaccades to the stimulus were obtained compared with a control session with no cue. In the two experimental blocks with noninformative cues, the reaction times of correct antisaccades were decreased when cue and stimulus were on at the same side, while large numbers of erratic prosaccades were again obtained when cue and stimulus were presented on opposite sides. These results suggest that the orienting mechanism elicited by a transient peripheral cue relates to the command and to the decision to make a proversus an antisaccade. Since the subjects reported that they could not prevent, or, moreover, in some cases did not even realize that they were making erratic prosaccades, we conclude that this orienting mechanism occurs automatically, being largely beyond voluntary control.     

The automatic extraction and use of information from cues and go signals in an antisaccade task

In a gap antisaccade task that exogenously cues the side that subjects should antisaccade to, subjects find it hard to look away from the suddenly appearing go signal. Surprisingly, subjects are unaware of the majority of the prosaccade errors they make, and these errors remain unrecognised even when corrected by a second saccade requiring twice the amplitude [Fischer B, Weber H (1992) in Exp Brain Res 89:415–424]. This paper presents an extended antisaccade task that investigates what information, if any, subjects extract from redundant cues and go signals. In Exp. 1, multiple saccade locations were introduced and the go signal specified the goal location. A redundant cue appeared, prior to the go signal, in the antisaccade goal location (valid) or in the alternative location on the same side (invalid). In Exp. 2, motivational value was assigned to the go signal. The use of multiple locations showed that subjects automatically extract irrelevant positional information from the cue, which affects the programming of subsequent correct and error saccades. When the cued location was also the goal location, antisaccade reaction times were significantly reduced. The results from Exp. 2 showed that subjects also extract information from the go signal. Errors made to a go signal associated with a higher monetary value were initiated significantly faster than those to a lower monetary value. This study has shown that the visual stimuli used in this antisaccade task do more than initiate orienting sets: Their properties can influence the programming of both accurate actions and errors.     

Females and attention to eye gaze: effects of the menstrual cycle

It is well known that an observer will attend to the location cued by another’s eye gaze and that in some circumstances, this effect is enhanced when the emotion expressed is threat-related. This study explored whether attention to the gaze of threat-related faces is potentiated in the luteal phase of the menstrual cycle when detection of threat is suggested to be enhanced, compared to the follicular phase. Female participants were tested on a gaze cueing task in their luteal (N = 13) or follicular phase (N = 15). Participants were presented with various emotional expressions with an averted eye gaze that was either spatially congruent or incongruent with a forthcoming target. Females in the luteal phase responded faster overall to targets on trials with a 200-ms stimulus onset asynchrony interval. The results suggest that during the luteal phase, females show a general and automatic hypersensitivity to respond to stimuli associated with socially and emotionally relevant cues. This may be a part of an adaptive biological mechanism to protect foetal development.     

Spatial orienting of attention simultaneously cued by automatic social and nonsocial cues

The appearance of a stimulus in the periphery and the direction of another person’s eye gaze have both been shown to automatically orient attention toward the stimulus and the gazed-at location, respectively. In the present experiment, we examined the effects of viewing both a peripheral stimulus and an eye gaze stimulus simultaneously in order to determine whether one is “more automatic” (i.e., faster, dominates) than the other and whether the two processes interact. Using a spatial cueing paradigm, we measured latency of localization of a target stimulus that was validly or invalidly cued by an uninformative (i.e., nonpredictive) peripheral cue, an uninformative eye gaze cue, or both simultaneously (double cue). We included a short and a long cue-target interval in order to investigate the early and late facilitatory and inhibitory effects of the two processes. Results demonstrated that when the double cues were consistent with each other (indicating the same target location), the effects, both early and late, were the same as when the peripheral cue was presented alone. When the double cues were inconsistent (indicating opposite target locations), the late effect was the same as the peripheral cue, but the early effect was intermediate between the two types of cues. Our results better support an interactive, rather than an additive relationship between social and nonsocial automatic orienting. The double cue conditions that showed similar effects to the peripheral cues suggest that the peripheral cue dominates.     

The development of grasping comprehension in infancy: covert shifts of attention caused by referential actions

An eye tracking paradigm was used to investigate how infants’ attention is modulated by observed goal-directed manual grasping actions. In Experiment 1, we presented 3-, 5-, and 7-month-old infants with a static picture of a grasping hand, followed by a target appearing at a location either congruent or incongruent with the grasping direction of the hand. The latency of infants gaze shift from the hand to the target was recorded and compared between congruent and incongruent trials. Results demonstrate a congruency effect from 5 months of age. A second experiment illustrated that the congruency effect of Experiment 1 does not extend to a visually similar mechanical claw (instead of the grasping hand). Together these two experiments describe the onset of covert attention shifts in response to manual actions and relate these findings to the onset of manual grasping.     

Differing effects of prosaccades and antisaccades on postural stability

The goal of the study was to examine the effect of different types of eye movements on postural stability. Ten healthy young adults (25 ± 3 years) participated in the study. Postural control was measured by the TechnoConcept© platform and recorded in Standard Romberg and Tandem Romberg conditions while participants performed five oculomotor tasks: two fixation tasks (central fixation cross, without and with distractors), two prosaccade tasks toward peripheral targets displayed 4° to the left or to the right of the fixation cross (reactive saccades induced by a gap 0 ms paradigm and voluntary saccades induced by an overlap 600 ms paradigm) and one antisaccade task (voluntary saccade made in the opposite direction of the visual target). The surface, the length, and the mean speed of the center of pressure were analyzed. We found that saccadic eye movements improved postural stability with respect to the fixation tasks. Furthermore, antisaccades were found to decrease postural stability compared to prosaccades (reactive as well as voluntary saccades). This result is in line with the U-shaped nonlinear model described by Lacour et al. (Neurophysiol Clin 38:411–421, 2008), showing that a secondary task performed during a postural task could increase (prosaccade task) or decrease (antisacade task) postural stability depending on its complexity. We suggest that the different degree of attentional resources needed for performing prosaccade or antisaccade tasks are, most likely, responsible for the different effect on postural control.     

Reduced activity within the dorsal endogenous orienting of attention network to fearful expressions in youth with disruptive behavior disorders and psychopathic traits

Using behavioral and blood oxygen level dependent (BOLD) response indices through functional magnetic resonance imaging (fMRI), the current study investigated whether youths with disruptive behavior disorders (conduct disorder and oppositional defiant disorder) plus psychopathic traits (DBD + PT) show aberrant sensitivity to eye gaze information generally and/or whether they show particular insensitivity to eye gaze information in the context of fearful expressions. The participants were 36 children and adolescents (ages 10-17 years); 17 had DBD + PT and 19 were healthy comparison subjects. Participants performed a spatial attention paradigm where spatial attention was cued by eye gaze in faces displaying fearful, angry, or neutral affect. Eye gaze sensitivity was indexed both behaviorally and as BOLD response. There were no group differences in behavioral response: both groups showed significantly faster responses if the target was in the congruent spatial direction indicated by eye gaze. Neither group showed a Congruence × Emotion interaction; neither group showed an advantage from the displayer's emotional expression behaviorally. However, the BOLD response revealed a significant Group × Congruence × Emotion interaction. The comparison youth showed increased activity within the dorsal endogenous orienting network (superior parietal lobule and inferior parietal sulcus) for fearful congruent relative to incongruent trials relative to the youth with DBD + PT. The results are discussed with reference to current models of DBD + PT and possible treatment innovations.     

Neuronal activity related to rule and conflict in macaque supplementary eye field

Neuronal activity in macaque supplementary eye field (SEF) is enhanced during performance of the antisaccade task. This could be related to the selection of targets by a difficult rule (move to a location diametrically opposite the cue) or to conflict between the automatic tendency to look at the cue and the voluntary intention to look away. To distinguish between rule- and conflict-based mechanisms of enhancement, we monitored neuronal activity in the SEF during performance of a delayed response task in which monkeys selected saccade targets in response to peripheral visual cues. In spatial trials, the monkey had to select as target the location marked by the cue. In color trials, the monkey had to select as target the location associated with the color of the cue. 'Color-congruent' trials resembled spatial trials in that saccades were directed to the location occupied by the cue. Nevertheless, many SEF neurons were sensitive to the rule being used, with the majority firing more strongly under the color-rule condition. 'Color-incongruent' trials resembled 'color-congruent' trials in that a color rule guided target selection. Nevertheless, many SEF neurons were sensitive to the spatial relation between cue and saccade, with the majority firing more strongly on trials in which they were incongruent. We conclude that neuronal activity in the SEF is enhanced in connection both with the use of a more difficult rule and with conflict.     

Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task.

The close relationship between saccadic eye movements and vision complicates the identification of neural responses associated with each function. Visual and saccade-related responses are especially closely intertwined in a subdivision of posterior parietal cortex, the lateral parietal area (LIP). We analyzed LIP neurons using an antisaccade task in which monkeys made saccades away from a salient visual cue. The vast majority of neurons reliably signaled the location of the visual cue. In contrast, most neurons had only weak, if any, saccade-related activity independent of visual stimulation. Thus, whereas the great majority of LIP neurons reliably encoded cue location, only a small minority encoded the direction of the upcoming saccade.     

Microstimulation of monkey dorsolateral prefrontal cortex impairs antisaccade performance

The dorsolateral prefrontal cortex (DLPFC) has been implicated in various cognitive functions, including response suppression. This function is frequently probed with the antisaccade task, which requires suppression of the automatic tendency to look toward a flashed peripheral stimulus (prosaccade), and instead generate a voluntary saccade to the mirror location. To test whether activity in the DLPFC is causally linked to antisaccade performance, we applied electrical microstimulation to sites in the DLPFC of two monkeys, while they performed randomly interleaved pro- and antisaccade trials. Microstimulation resulted in significantly longer saccadic reaction times for ipsilaterally directed prosaccades and antisaccades, and increased the error rate on ipsilateral antisaccade trials. These findings provide causal evidence that activity in the DLPFC influences saccadic eye movements.