Covert orienting of attention in 3-month-old infants: The case of biological motion

Humans attend to different positions in the space either by moving their eyes or by moving covertly their attention. The development of covert attention occurs during the first year of life. According to Colombo’s model of attention (2001), within the first years there is a significant change in infants’ visuo-spatial orienting mechanisms, from a predominantly overt form to a covert orienting starting from 4 to 5 months of life. The use of non-invasive brain imaging techniques can shed light on the origin of such mechanisms. In particular, EEG and ERP studies can directly investigate the neural correlates of covert attention in young infants. The present study investigated the neural correlates of covert attention employing a visuo-spatial cueing paradigm in 3-month-old infants. Infants were presented with a central point-light walker (PLD) followed by a single peripheral target. The target appeared randomly at a position either congruent or incongruent with the walking direction of the cue. We examined infants’ target-locked P1 component and the saccade latencies toward the peripheral target. Results showed that the P1 component was larger in response to congruent than to incongruent targets and saccade latencies were faster for congruent rather than incongruent trials. Moreover, the facilitation in processing sensory information (priming effects) presented at the cued spatial location occurs even before the onset of the oculomotor response, suggesting that covert attention is present before 4 months of age. Overall, this study highlights how ERPs method could help researchers at investigating the neural basis of attentional mechanisms in infants.     

Sensitivity to auditory‐tactile colocation in early infancy

An ability to detect the common location of multisensory stimulation is essential for us to perceive a coherent environment, to represent the interface between the body and the external world, and to act on sensory information. Regarding the tactile environment “at hand”, we need to represent somatosensory stimuli impinging on the skin surface in the same spatial reference frame as distal stimuli, such as those transduced by vision and audition. Across two experiments we investigated whether 6‐ (n = 14; Experiment 1) and 4‐month‐old (n = 14; Experiment 2) infants were sensitive to the colocation of tactile and auditory signals delivered to the hands. We recorded infants’ visual preferences for spatially congruent and incongruent auditory‐tactile events delivered to their hands. At 6 months, infants looked longer toward incongruent stimuli, whilst at 4 months infants looked longer toward congruent stimuli. Thus, even from 4 months of age, infants are sensitive to the colocation of simultaneously presented auditory and tactile stimuli. We conclude that 4‐ and 6‐month‐old infants can represent auditory and tactile stimuli in a common spatial frame of reference. We explain the age‐wise shift in infants’ preferences from congruent to incongruent in terms of an increased preference for novel crossmodal spatial relations based on the accumulation of experience. A comparison of looking preferences across the congruent and incongruent conditions with a unisensory control condition indicates that the ability to perceive auditory‐tactile colocation is based on a crossmodal rather than a supramodal spatial code by 6 months of age at least.     

Automatic attentional orienting to other people’s gaze in schizophrenia

Explicit tests of social cognition have revealed pervasive deficits in schizophrenia. Less is known of automatic social cognition in schizophrenia. We used a spatial orienting task to investigate automatic shifts of attention cued by another person’s eye gaze in 29 patients and 28 controls. Central photographic images of a face with eyes shifted left or right, or looking straight ahead, preceded targets that appeared left or right of the cue. To examine automatic effects, cue direction was non-predictive of target location. Cue–target intervals were 100, 300, and 800?ms. In non-social control trials, arrows replaced eye-gaze cues. Both groups showed automatic attentional orienting indexed by faster reaction times (RTs) when arrows were congruent with target location across all cue–target intervals. Similar congruency effects were seen for eye-shift cues at 300 and 800?ms intervals, but patients showed significantly larger congruency effects at 800?ms, which were driven by delayed responses to incongruent target locations. At short 100-ms cue–target intervals, neither group showed faster RTs for congruent than for incongruent eye-shift cues, but patients were significantly slower to detect targets after direct-gaze cues. These findings conflict with previous studies using schematic line drawings of eye-shifts that have found automatic attentional orienting to be reduced in schizophrenia. Instead, our data indicate that patients display abnormalities in responding to gaze direction at various stages of gaze processing—reflected by a stronger preferential capture of attention by another person’s direct eye contact at initial stages of gaze processing and difficulties disengaging from a gazed-at location once shared attention is established.     

Neural correlates of perceptual narrowing in cross‐species face‐voice matching

Integrating the multisensory features of talking faces is critical to learning and extracting coherent meaning from social signals. While we know much about the development of these capacities at the behavioral level, we know very little about the underlying neural processes. One prominent behavioral milestone of these capacities is the perceptual narrowing of face–voice matching, whereby young infants match faces and voices across species, but older infants do not. In the present study, we provide neurophysiological evidence for developmental decline in cross‐species face–voice matching. We measured event‐related brain potentials (ERPs) while 4‐ and 8‐month‐old infants watched and listened to congruent and incongruent audio‐visual presentations of monkey vocalizations and humans mimicking monkey vocalizations. The ERP results indicated that younger infants distinguished between the congruent and the incongruent faces and voices regardless of species, whereas in older infants, the sensitivity to multisensory congruency was limited to the human face and voice. Furthermore, with development, visual and frontal brain processes and their functional connectivity became more sensitive to the congruence of human faces and voices relative to monkey faces and voices. Our data show the neural correlates of perceptual narrowing in face–voice matching and support the notion that postnatal experience with species identity is associated with neural changes in multisensory processing ( Lewkowicz & Ghazanfar, 2009 ).     

The attentional ‘zoom‐lens’ in 8‐month‐old infants

The spatial attention mechanisms of orienting and zooming cooperate to properly select visual information from the environment and plan eye movements accordingly. Despite the fact that orienting ability has been extensively studied in infancy, the zooming mechanism – namely, the ability to distribute the attentional resources to a small or large portion of the visual field – has never been tested before. The aim of the present study was to evaluate the attentional zooming abilities of 8‐month‐old infants. An eye‐tracker device was employed to measure the saccadic latencies (SLs) at the onset of a visual target displayed at two eccentricities. The size of the more eccentric target was adjusted in order to counteract the effect of cortical magnification. Before the target display, attentional resources were automatically focused (zoom‐in) or spread out (zoom‐out) by using a small or large cue, respectively. Two different cue–target intervals were also employed to measure the time course of this attentional mechanism. The results showed that infants' SLs varied as a function of the cue size. Moreover, a clear time course emerged, demonstrating that infants can rapidly adjust the attentional focus size during a pre‐saccadic temporal window. These findings could serve as an early marker for neurodevelopmental disorders associated with attentional zooming dysfunction such as autism and dyslexia.     

Developmental changes in the control of saccadic eye movements in response to directional eye gaze and arrows

We investigated developmental differences in oculomotor control between 10-year-old children and adults using a central interference task. In this task, the colour of a fixation point instructed participants to saccade either to the left or to the right. These saccade directions were either congruent or incongruent with two types of distractor cue: either the direction of eye gaze of a centrally presented schematic face, or the direction of arrows. Children had greater difficulties inhibiting the distractor cues than did adults, which revealed itself in longer saccade latencies for saccades that were incongruent with the distractor cues as well as more errors on these incongruent trials than on congruent trials. Counter to our prediction, in terms of saccade latencies, both children and adults had greater difficulties inhibiting the arrow than the eye gaze distractors.     

Developmental changes in the control of saccadic eye movements in response to directional eye gaze and arrows

We investigated developmental differences in oculomotor control between 10-year-old children and adults using a central interference task. In this task, the colour of a fixation point instructed participants to saccade either to the left or to the right. These saccade directions were either congruent or incongruent with two types of distractor cue: either the direction of eye gaze of a centrally presented schematic face, or the direction of arrows. Children had greater difficulties inhibiting the distractor cues than did adults, which revealed itself in longer saccade latencies for saccades that were incongruent with the distractor cues as well as more errors on these incongruent trials than on congruent trials. Counter to our prediction, in terms of saccade latencies, both children and adults had greater difficulties inhibiting the arrow than the eye gaze distractors.     

What gaze adds to arrows: Changes in attentional response to gaze versus arrows in childhood and adolescence

From early ages, gaze acts as a cue to infer the interests, behaviours, thoughts and emotions of social partners. Despite sharing attentional properties with other non-social directional stimuli, such as arrows, gaze produces unique effects. A spatial interference task revealed this dissociation. The direction of arrows was identified faster on congruent than on incongruent direction-location trials. Conversely, gaze produced a reversed congruency effect (RCE), with faster identifications on incongruent than congruent trials. To determine the emergence of these gaze-specific attentional mechanisms, 214 Spanish children (4–17 years) divided into 6 age groups, performed the aforementioned task across three experiments. Results showed stimulus-specific developmental trajectories. Whereas the standard effect of arrows was unaffected by age, gaze shifted from an arrow-like effect at age 4 to a gaze-specific RCE at age 12. The orienting mechanisms shared by gaze and arrows are already present in 4-year olds and, throughout childhood, gaze becomes a special social cue with additional attentional properties. Besides orienting attention to a direction, as arrows would do, gaze might orient attention towards a specific object that would be attentionally selected. Such additional components may not fully develop until adolescence. Understanding gaze-specific attentional mechanisms may be crucial for children with atypical socio-cognitive development.     

Gaze cueing as a function of perceived gaze direction

Previous studies have found that attention is automatically oriented in the direction of other people's gaze. This study directly investigated whether the perceiving gaze direction modulates the orienting of observers' attention. Gaze perception was manipulated by changing the face context (head orientation) of the gaze cue: the perceived gaze angle was increased (or decreased) when the head and gaze are congruent (or incongruent), while the local‐feature information of the eye region was preserved for all stimuli. The results showed that gaze‐cueing effects were enhanced when the perceived gaze direction was averted more toward left or right, and reduced when the perceived gaze direction was closer to direct gaze. The results suggest that gaze‐cueing effects are based on mechanisms specialized for gaze perception, and the magnitude of gaze‐cueing effects was probably a function of the perceived gaze direction.     

Does crossmodal correspondence modulate the facilitatory effect of auditory cues on visual search?

The ??pip-and-pop effect?? refers to the facilitation of search for a visual target (a horizontal or vertical bar whose color changes frequently) among multiple visual distractors (tilted bars also changing color unpredictably) by the presentation of a spatially uninformative auditory cue synchronized with the color change of the visual target. In the present study, the visual stimuli in the search display changed brightness instead of color, and the crossmodal congruency between the pitch of the auditory cue and the brightness of the visual target was manipulated. When cue presence and cue congruency were randomly varied between trials (Experiment 1), both congruent cues (low-frequency tones synchronized with dark target states or high-frequency tones synchronized with bright target states) and incongruent cues (the reversed mapping) facilitated visual search performance equally, relative to a no-cue baseline condition. However, when cue congruency was blocked and the participants were informed about the pitch?Cbrightness mapping in the cue-present blocks (Experiment 2), performance was significantly enhanced when the cue and target were crossmodally congruent as compared to when they were incongruent. These results therefore suggest that the crossmodal congruency between auditory pitch and visual brightness can influence performance in the pip-and-pop task by means of top-down facilitation.     

Electrophysiological correlates of crossmodal visual distractor congruency effects: Evidence for response conflict

To investigate the basis of crossmodal visual distractor congruency effects, we recorded event-related brain potentials (ERP) while participants performed a tactile location-discrimination task. Participants made speeded tactile location-discrimination responses to tactile targets presented to the index fingers or thumbs while ignoring simultaneously presented task-irrelevant visual distractor stimuli at either the same (congruent) or a different (incongruent) location. Behavioural results were in line with previous studies, showing slowed response times and increased error rates on incongruent compared with congruent visual distractor trials. To clarify the effect of visual distractors on tactile processing, concurrently recorded ERPs were analyzed for poststimulus, preresponse, and postresponse modulations. An enhanced negativity was found in the time range of the N2 component on incongruent compared with congruent visual distractor trials prior to correct responses. In addition, postresponse ERPs showed the presence of error-related negativity components on incorrect-response trials and enhanced negativity for congruent-incorrect compared with incongruent-incorrect trials. This pattern of ERP results has previously been related to response conflict (Yeung, Botvinick, & Cohen, 2004). Importantly, no modulation of early somatosensory ERPs was present prior to the N2 time range, which may have suggested the contribution of other perceptual or postperceptual processes to crossmodal congruency effects. Taken together, our results suggest that crossmodal visual distractor effects are largely due to response conflict.     

情境特异比例一致变化对冲突效应的影响

采用Hedge和Marsh任务与比例一致性操纵相结合,分别以刺激的空间位置和形状作为比例一致操纵的情境线索,考察刺激-反应联结学习与注意调节在比例一致效应中的作用。结果发现,在情境比例一致操纵下,冲突效应的效应量受到比例一致操纵的影响产生反转。表明刺激-反应联结学习在情境特异比例一致效应中起到主要作用。     

Development of saccade target selection in infants.

To investigate the development of the target selection process for saccade generation, saccade latencies toward one of two targets were compared with those toward a target presented alone, under conditions where the timing of fixation stimulus offset was varied. 12 2-mo.-olds (7 boys and 5 girls), 12 3-mo.-olds (6 boys and 6 girls), and 12 5-mo.-olds (8 boys and 4 girls) participated. The latencies were longer when two saccade targets were presented on the left and right sides of the display (Double-target condition) than when one target was presented either on the left or right side of the display (Single-target condition). The difference between the Single and Double-target conditions tended to be larger in 2-mo. old infants than in 5-mo.-old infants when a central fixation target remained on after the onset of peripheral stimuli (Overlap condition). However, there was no difference between the 2-mo.-olds and the 5-mo.-olds when the fixation target was turned off before the peripheral stimuli were presented (Gap condition). The results provided evidence of the maturational development of a target selection process for saccade generation during 2 to 5 mo. of age.     

Saccade-stepping interactions revise the motor plan for obstacle avoidance

The authors used a stimulus-response compatibility paradigm to assess the effect of changing the estimated time to obstacle contact. A limb-selection cue was presented in different phases of gait to young (n = 5) and to older (n = 4) adults while they were moving toward a foam obstacle in the walking path. A downward saccade was initiated after the cue; the saccade typically occurred during the stance phase of the target limb (the foot cued to lead the step over the obstacle). The mean saccade-step latency after the cue was on the order of -500 ms in both young and elderly participants. On reaching the obstacle, both groups generated an upward saccade approximately -300 ms before target footlift in both groups. Saccades following the limb-selection cue appeared to direct the gaze toward footfall targets just beyond the obstacle, whereas saccades generated just before obstacle footlift moved the gaze to the forward-looking direction. The elderly had significantly longer saccade-trailing-footlift latencies and prolonged gaze-fixation times than did the younger adults. Transient disruptions in optical flow appeared to be necessary for successful obstacle-avoidance behavior when there was an unexpected change in the estimated time to obstacle contact.     

Saccade-Stepping Interactions Revise the Motor Plan for Obstacle Avoidance

The authors used a stimulus-response compatibility paradigm to assess the effect of changing the estimated time to obstacle contact. A limb-selection cue was presented in different phases of gait to young (n = 5) and to older (n = 4) adults while they were moving toward a foam obstacle in the walking path. A downward saccade was initiated after the cue; the saccade typically occurred during the stance phase of the target limb (the foot cued to lead the step over the obstacle). The mean saccade-step latency after the cue was on the order of ?500 ms in both young and elderly participants. On reaching the obstacle, both groups generated an upward saccade approximately ?300 ms before target footlift in both groups. Saccades following the limb-selection cue appeared to direct the gaze toward footfall targets just beyond the obstacle, whereas saccades generated just before obstacle footlift moved the gaze to the forward-looking direction. The elderly had significantly longer saccade-trailing-footlift latencies and prolonged gaze-fixation times than did the younger adults. Transient disruptions in optical flow appeared to be necessary for successful obstacle-avoidance behavior when there was an unexpected change in the estimated time to obstacle contact.     

Positive and negative emotions modulate attention allocation in color-flanker task processing: Evidence from event related potentials

The purpose of this study was to explore the effects of emotions in conflict processing. Behavioral and event related potential (ERP) data were acquired from twenty participants while they were performing a color-flanker task, in which the stimuli were emotional and neutral words. Through temporal principal component analysis (PCA) of ERP, three PCA components were extracted with their time windows mapped to three ERP components: N1, N2 and P3. Further analysis revealed, when the stimuli were the positive words, N1 was marginally greater for the congruent condition than for the incongruent condition (p = .06); while the stimuli were the negative words, N1 was greater for the incongruent condition than for the congruent condition (p = .02); however, no significant interaction effect involving the valence of words (positive vs. negative) and the color congruency (congruent vs. incongruent) was found on N2, P3 and the behavior data. The result suggested that negative emotion might lead to more attention allocation in the incongruent processing, while positive emotion might lead to more attention allocation in the congruent processing. Furthermore, ERP source analysis in the present study confirmed anterior cingulate cortex was involved in the conflict monitoring mechanism.     

Pupillometry reveals communication‐induced object expectations in 12‐ but not 8‐month‐old infants

Several interaction‐based and looking‐time studies suggest that 1‐year‐old infants understand the referential nature of deictic gestures. However, these studies have not unequivocally established that referential gestures induce object expectations in infants prior to encountering a referent object, and have thus remained amenable to simpler attentional highlighting interpretations. The current study tested whether nonlinguistic referential communication induces object expectations in infants by using a novel pupil dilation paradigm. In Experiment 1, 12‐month‐olds watched videos of a protagonist who either pointed communicatively toward an occluder in front of her or remained still. At test, the occluder opened to reveal one of two outcomes: an empty surface or a toy. Results showed that infants’ pupils were larger for the unexpected outcome of an empty surface following a point compared to the control condition (an empty surface following no point). These differences were not caused by differences in looking times or directions. In Experiment 2, an attention‐directing nonsocial control cue replaced the referential communication. The cue did direct 12‐month‐olds’ attention to the occluder, but it did not induce an object expectation. In Experiment 3, we tested 8‐month‐olds in the setting of Experiment 1. In contrast to 12‐month‐olds, 8‐month‐olds did not reveal object expectations following communication. Findings demonstrate that communicative pointing acts induce object expectations at 12 months of age, but not at 8 months of age, and that these expectations are specific to a referential‐communicative as opposed to an attention‐directing nonsocial cue.     

Contrast polarity of eyes modulates gaze‐cueing effect1

Two experiments using a modified Posner‐type visual cueing paradigm tested the prediction that detecting the darker region of the eyes of another's gaze triggers a reflexive orienting of the observer in the direction of the gaze. A target was presented in the left or right visual‐field following a gaze‐cue with positive or negative‐image polarity (Experiment 1). In Experiment 2, the polarity of the eyes was manipulated independently of the negative polarity of the face (eye‐positive or eye‐negative‐image polarity conditions). The results showed that the response to the target presented at the side the eyes gazed toward was faster than for the target presented at the other side in the positive polarity condition (Experiment 1), whereas, in the negative polarity condition, the gaze‐cuing effect was not found. In Experiment 2, in the eye‐negative condition, a reversed gaze‐cueing effect appeared, whereas in the eye‐positive polarity condition, a typical gaze‐cueing effect was obtained. These findings suggested that the reflexive orienting of the observer shifts toward the position indicated by the darker region of the other's eyes.     

Action effects in saccade control

According to the ideomotor principle, action preparation involves the activation of associations between actions and their effects. However, there is only sparse research on the role of action effects in saccade control. Here, participants responded to lateralized auditory stimuli with spatially compatible saccades toward peripheral targets (e.g., a rhombus in the left hemifield and a square in the right hemifield). Prior to the imperative auditory stimulus (e.g., a left tone), an irrelevant central visual stimulus was presented that was congruent (e.g., a rhombus), incongruent (e.g., a square), or unrelated (e.g., a circle) to the peripheral saccade target (i.e., the visual effect of the saccade). Saccade targets were present throughout a trial (Experiment 1) or appeared after saccade initiation (Experiment 2). Results showed shorter response times and fewer errors in congruent (vs. incongruent) conditions, suggesting that associations between oculomotor actions and their visual effects play an important role in saccade control.     

Emotional attention: effects of emotion and gaze direction on overt orienting of visual attention

In the present study we considered the two factors that have been advocated for playing a role in emotional attention: perception of gaze direction and facial expression of emotions. Participants performed an oculomotor task in which they had to make a saccade towards one of the two lateral targets, depending on the colour of the fixation dot which appeared at the centre of the computer screen. At different time intervals (stimulus onset asynchronies, SOAs: 50,100,150 ms) following the onset of the dot, a picture of a human face (gazing either to the right or to the left) was presented at the centre of the screen. The gaze direction of the face could be congruent or incongruent with respect to the location of the target, and the expression could be neutral or angry. In Experiment 1 the facial expressions were presented randomly in a single block, whereas in Experiment 2 they were shown in separate blocks. Latencies for correct saccades and percentage of errors (saccade direction errors) were considered in the analyses. Results showed that incongruent trials determined a significantly higher percentage of saccade direction errors with respect to congruent trials, thus confirming that gaze direction, even when task-irrelevant, interferes with the accuracy of the observer’s oculomotor behaviour. The angry expression was found to hold attention for a longer time with respect to the neutral one, producing delayed saccade latencies. This was particularly evident at 100 ms SOA and for incongruent trials. Emotional faces may then exert a modulatory effect on overt attention mechanisms.