Publications of Johnson, M.H.

Motor system activation reveals infants’ on-line prediction of others’ goals

Despite much research demonstrating infants’ abilities to attribute goals to others’ actions, it is unclear whether infants can generate on-line predictions about action outcomes, an ability crucial for the human propensity to cooperate and collaborate with others. This lack of evidence is mainly due to methodological limitations restricting the interpretation of behavioral data. Here, we exploited the fact that observers’ motor systems are recruited during the observation of goal-directed actions. We presented 9-month-old infants with part of an action. For this action to be interpreted as goal directed, the infants would need to predict an outcome for the action. Measuring the attenuation of the sensorimotor alpha signal during observation of action, we found that infants exhibited evidence of motor activation only if the observed action permitted them to infer a likely outcome. This result provides evidence for on-line goal prediction in infancy, and our method offers a new way to explore infants’ cognitive abilities.

Neural correlates of eye gaze processing in the infant broader autism phenotype

Background: Studies of infant siblings of children diagnosed with autism have allowed for a prospective approach to study the emergence of autism in infancy and revealed early behavioral characteristics of the broader autism phenotype. In view of previous findings of atypical eye gaze processing in children and adults with autism, the aim of this study was to examine the early autism phenotype in infant siblings of children diagnosed with autism spectrum disorder (sib-ASD), focusing on the neural correlates of direct compared with averted gaze. Methods: A group of 19 sib-ASD was compared with 17 control infants with no family history of ASD (mean age = 10 months) on their response to direct versus averted gaze in static stimuli. Results: Relative to the control group, the sib-ASD group showed prolonged latency of the occipital P400 event-related potentials component in response to direct gaze, but they did not differ in earlier components. Similarly, time-frequency analysis of high-frequency oscillatory activity in the gamma band showed group differences in response to direct gaze, where induced gamma activity was late and less persistent over the right temporal region in the sib-ASD group. Conclusion: This study suggests that a broader autism phenotype, which includes an atypical response to direct gaze, is manifest early in infancy.

Rapid orienting toward face-like stimuli with gaze-relevant contrast information

Human faces under natural illumination, and human eyes in their unique morphology, include specific contrast polarity relations that face-detection mechanisms could capitalise on. Newborns have been shown to preferentially orient to simple face-like patterns only when they contain face- or gaze-relevant contrast. We investigated whether human adults show similar preferential orienting towards schematic face-like stimuli, and whether this effect depends on the contrast polarity of the stimuli. In two experiments we demonstrate that upright schematic face-like patterns elicit faster eye movements in adult humans than inverted ones, and that this Occurs only if they contain face- or gaze-relevant contrast information in the whole stimulus or in the eye region only. These results suggest that primitive mechanisms underlying the orienting bias towards faces and eyes influence and modulate social cognition not just in infants but in adults as well.

Predictive motor activation during action observation in human infants

Certain regions of the human brain are activated both during action execution and action observation. This so-called ‘mirror neuron system’ has been proposed to enable an observer to understand an action through a process of internal motor simulation. Although there has been much speculation about the existence of such a system from early in life, to date there is little direct evidence that young infants recruit brain areas involved in action production during action observation. To address this question, we identified the individual frequency range in which sensorimotor alpha-band activity was attenuated in nine-month-old infants’ electroencephalographs (EEGs) during elicited reaching for objects, and measured whether activity in this frequency range was also modulated by observing others’ actions. We found that observing a grasping action resulted in motor activation in the infant brain, but that this activity began prior to observation of the action, once it could be anticipated. These results demonstrate not only that infants, like adults, display overlapping neural activity during execution and observation of actions, but that this activation, rather than being directly induced by the visual input, is driven by infants’ understanding of a forthcoming action. These results provide support for theories implicating the motor system in action prediction.

Freeze-Frame: A new infant inhibition task and its relation to frontal cortex tasks during infancy and early childhood

The current study investigated a new, easily administered, visual inhibition task for infants termed the Freeze-Frame task. In the new task, 9-month-olds were encouraged to inhibit looks to peripheral distractors. This was done by briefly freezing a central animated stimulus when infants looked to the distractors. Half of the trials presented an engaging central stimulus, and the other half presented a repetitive central stimulus. Three measures of inhibitory function were derived from the task and compared with performance on a set of frontal cortex tasks administered at 9 and 24 months of age. As expected, infants' ability to learn to selectively inhibit looks to the distractors at 9 months predicted performance at 24 months. However, performance differences in the two Freeze-Frame trial types early in the experiment also turned out to be an important predictor. The results are discussed in terms of the validity of the Freeze-Frame task as an early measure of different components of inhibitory function. (C) 2007 Elsevier Inc. All rights reserved.

Understanding the referential nature of looking: Infants' preference for object-directed gaze

In four experiments, we investigated whether 9-month-old infants are sensitive to the relationship between gaze direction and object location and whether this sensitivity depends on the presence of communicative cues like eye contact. Infants observed a face, which repeatedly shifted its eyes either toward, or away from, unpredictably appearing objects. We found that they looked longer at the face when the gaze shifts were congruent with the location of the object. A second experiment ruled out that this effect was simply due to spatial congruency, while a third and a fourth experiment revealed that a preceding period of eye contact is required to elicit the gaze-object congruency effect. These results indicate that infants at this age can encode eye direction in referential terms in the presence of communication cues and are biased to attend to scenes with object-directed gaze. (c) 2008 Elsevier B.V. All rights reserved.

Distinct processing of objects and faces in the infant brain

Previous work has shown that gamma-band electroencephalogram oscillations recorded over the posterior cortex of infants play a role in maintaining object representations during occlusion. Although it is not yet known what kind of representations are reflected in these oscillations, behavioral data suggest that young infants maintain spatiotemporal (but not featural) information during the occlusion of graspable objects, and surface feature (but not spatiotemporal) information during the occlusion of faces. To further explore this question, we presented infants with an occlusion paradigm in which they would, on half of the trials, see surface feature violations of either a face or an object. Based on previous studies, we predicted higher gamma-band activation when infants were presented with a surface feature violation of a face, but not of an object. These results were confirmed. A further analysis revealed that whereas infants exhibited a significant increase in gamma during the occlusion of an object (as reported in previous studies), no such increase was evident during the occlusion of a face. These data suggest markedly different processing of objects and faces in the infant brain and, furthermore, indicate that the representation underpinned by the posterior gamma increase may contain only spatiotemporal information.

Social perception in the infant brain: gamma oscillatory activity in response to eye gaze

Gamma band oscillatory brain activity was measured to examine the neural basis of 4-month-old infants’ perception of eye gaze direction. Infants were presented with photographic images of upright and inverted female faces directing their gaze towards them or to the side. Direct gaze compared to averted gaze in upright faces elicited increased early evoked gamma activity at occipital channels indicating enhanced neural processing during the earliest steps of face encoding. Direct gaze also elicited a later induced gamma burst over right prefrontal channels, suggesting that eye contact detection might recruit very similar cortical regions as in adults. An induced gamma burst in response to averted gaze was observed over right posterior regions, which might reflect neural processes associated with shifting spatial attention. Inverted faces did not produce such effects, confirming that the gamma band oscillations observed in response to gaze direction are specific to upright faces. These data demonstrate the use of gamma band oscillations in examining the development of social perception and suggest an early specialization of brain regions known to process eye gaze.

Investigation of depth dependent changes in cerebral haemodynamics during face perception in infants

Near-infrared spectroscopy has been used to record oxygenation changes in the visual cortex of 4 month old infants. Our in-house topography system, with 30 channels and 3 different source–detector separations, recorded changes in the concentration of oxy-, deoxy- and total haemoglobin (HbO2, HHb and HbT) in response to visual stimuli (face, scrambled visual noise and cartoons as rest). The aim of this work was to demonstrate the capability of the system to spatially localize functional activation and study the possibility of depth discrimination in the haemodynamic response. The group data show both face stimulation and visual noise stimulation induced significant increases in HbO2 from rest, but the increase in HbO2 with face stimulation was not significantly different from that seen with visual noise stimulation. The face stimuli induced increases in HbO2 were spread across a greater area across all depths than visual noise induced changes. In results from a single subject there was a significant increase of HbO2 in the inferior area of the visual cortex in response to both types of stimuli, and a larger number of channels (source–detector pairs) showed HbO2 increase to face stimuli, especially at the greatest depth. Activation maps were obtained using 3D reconstruction methods on multi source–detector separation optical topography data.

Common-onset visual masking in infancy: Behavioral and electrophysiological evidence

Common-onset visual masking (COVM) occurs when a mask and a target have common onset but delayed offset, with the mask persisting beyond the duration of the target [Di Lollo, V., Enns, J. T., & Rensink, R. A. Competition for consciousness among visual events: The psychophysics of reentrant visual events. Journal of Experimental Psychology: General, 1-99, 481-507, 2000]. We report the first behavioral and electrophysiological evidence of COVM in infants. An initial behavioral Study included a familiarization phase during which a visual pattern (the target) surrounded by four black dots (the mask) was flashed 15 times to the infant. In the "unmasked" condition, the mask disappeared with the target. In the "masked" condition, the mask remained on the screen after deletion of the target for a further 93 msec. During the test phase, the familiar target pattern was paired with a new pattern. infants in the unmasked condition showed a significant familiarity preference, suggesting that they had encoded the target during familiarization, whereas those in the masked condition showed no preference, suggesting that they had not encoded the target during familiarization. In the second experiment, high-density event-related potentials were used to investigate the electrophysiological pattern of activity that accompanies COVM. Six-month-old infants viewed both masked and unmasked conditions. Electrophysiological data indicated that over posterior channels the masked condition elicited a larger amplitude positive wave around 300 msec after stimulus onset than trials in the unmasked condition.

Newborns' preference for face-relevant stimuli: Effects of contrast polarity

There is currently no agreement as to how specific or general are the mechanisms underlying newborns' face preferences. We address this issue by manipulating the contrast polarity of schematic and naturalistic face-related images and assessing the preferences of newborns. We find that for both schematic and naturalistic face images, the contrast polarity is important. Newborns did not show a preference for an upright face-related image unless it was composed of darker areas around the eyes and mouth. This result is consistent with either sensitivity to the shadowed areas of a face with overhead (natural) illumination and/or to the detection of eye contact.

Oscillatory activity in the infant brain reflects object maintenance

The apparent failure of infants to understand "object permanence" by reaching for hidden objects is perhaps the most striking and debated phenomenon in cognitive development. Of particular interest is the extent to which infants perceive and remember objects in a similar way to that of adults. Here we report two findings that clarify infant object processing. The first is that 6-mo-old infants are sensitive to visual cues to occlusion, particularly gradual deletion. The second finding is that oscillatory electroencephalogram activity recorded over right temporal channels is involved in object maintenance. This effect occurs only after disappearance in a manner consistent with occlusion and the object's continued existence.

Mechanisms of eye gaze perception during infancy

Previous work has shown that infants are sensitive to the direction of gaze of another's face, and that gaze direction can cue attention. The present study replicates and extends results on the ERP correlates of gaze processing in 4-month-olds. In two experiments, we recorded ERPs while 4-month-olds viewed direct and averted gaze within the context of averted and inverted heads. Our results support the previous finding that cortical processing of faces in infants is enhanced when accompanied by direct gaze. However, this effect is only found when eyes are presented within the context of an upright face.

Representing occluded objects in the human infant brain

One of the most striking phenomena in cognitive development has been the apparent failure of infants to show 'object permanence' in manual reaching tasks although they show evidence for representing hidden objects in studies measuring looking times. We report a neural correlate of object permanence in six-month-old infants: a burst of gamma-band EEG activity over the temporal lobe that occurs during an occlusion event and when an object is expected to appear from behind an occluder. We interpret this burst as being related to the infants' mental representation of the occluded object.

Eye contact detection in humans from birth

Making eye contact is the most powerful mode of establishing a communicative link between humans. During their first year of life, infants learn rapidly that the looking behaviors of others conveys significant information. Two experiments were carried out to demonstrate special sensitivity to direct eye contact from birth. The first experiment tested the ability of 2- to 5-day-old newborns to discriminate between direct and averted gaze. In the second experiment, we measured 4-month-old infants' brain electric activity to assess neural processing of faces when accompanied by direct (as opposed to averted) eye gaze. The results show that, from birth, human infants prefer to look at faces that engage them in mutual gaze and that, from an early age, healthy babies show enhanced neural processing of direct gaze. The exceptionally early sensitivity to mutual gaze demonstrated in these studies is arguably the major foundation for the later development of social skills.

Differential frontal cortex activation before anticipatory and reactive saccades in infants

Neural correlates of anticipatory and reactive saccades were studied in 4-month-old infants by recording high-density event-related potentials. Infants were presented with a fixed sequence of stimulus presentation to which they rapidly showed anticipatory saccades, as well as continuing with some reactive (stimulus-driven) saccades. As in a previous study, no clear evidence was found for adultlike, saccade-related potentials, although some presaccadic differences between reactive and anticipatory saccades were observed. Infants also showed different stimulus offset-related effects preceding the 2 types of trials with a right-frontal positivity when an anticipatory look follows, but only left-frontal positivity when a reactive saccade follows.

Disordered visual processing and oscillatory brain activity in autism and Williams Syndrome

Two developmental disorders, autism and Williams syndrome, are both commonly described as having difficulties in integrating perceptual features, i.e. binding spatially separate elements into a whole. It is already known that healthy adults and infants display electroencephalographic (EEG) gamma -band bursts (around 40 Hz) when the brain is required to achieve such binding. Here we explore gamma -band EEG in autism and Williams Syndrome and demonstrate differential abnormalities in the two phenotypes. We show that despite putative processing similarities at the cognitive level, binding in Williams syndrome and autism can be dissociated at the neurophysiological level by different abnormalities in underlying brain oscillatory activity. Our study is the first to identify that binding-related gamma EEG can be disordered in humans. NeuroReport 12:2697-2700 (C) 2001 Lippincott Williams & Wilkins.

Electrophysiological correlates of category goodness

We report the results obtained from a behavioural and electrophysiological study. A synthesised continuum going from labial /ba/ to retroflex /da/ through dental /da/ was tested for category goodness. Native English speakers rated different tokens from each category as good, bad or ambiguous. The results showed that not all of the representatives of each category were ideal and that the categories tested have an internal structure. The electrophysiological study evaluated whether event related potentials (ERPs) mirrored the goodness judgements. During a passive oddball task, the same participants were exposed to native /ba/-/da/, Hindi dental /da/-retroflex /da/ and within-category /ba/-/ba/ contrasts. Results showed that participants pre-attentively perceive the differences in all cases, as shown by mis-match negativities (MMN), late positive deflections (LPD) or greater N1 and/or P2 components for deviant stimuli. Acoustic sensitivities, categorical perception and category goodness all contributed to the waveforms obtained. We attribute the ERP effects to a combination of (1) prototypes built from initial sensitivities, (2) reinforcement with exposure to one's native language and (3) no permanent loss of the initial boundaries explains the effects observed. (C) 2000 Elsevier Science B.V. All rights reserved.

Neural correlates of saccade planning in infants: A high-density ERP study

Neural correlates of saccade planning in B-month-old infants were investigated by high-density event-related potentials. Subjects made saccades to a target stimulus following a time gap from fixation stimulus offset (gap trials) or with the fixation stimulus still present (overlap trials). Like adults, infants were slower to make a saccade to the target when the fixation stimulus was still present. Strikingly, infants did not show clear evidence of the pre-saccadic components observed in adults which are thought to reflect cortical saccade planning processes. They did, however, show a left frontal positivity, which we suggest reflects cortical disinhibition of the colliculus initiated by fixation stimulus offset, and clear post-saccadic lambda waves. These results indicate that the frontal cortex already plays a role in action control by 6 months of age, while other aspects of cortical action planning may not yet be present in certain task situations.