Nathan Caruana

A frontotemporoparietal network common to initiating and responding to joint attention bids

Joint attention is a fundamental cognitive ability that supports daily interpersonal relationships and communication. The Parallel Distributed Processing model (PDPM) postulates that responding to (RJA) and initiating (IJA) joint attention are predominantly supported by posterior-parietal and frontal regions respectively. It also argues that these neural networks integrate during development, supporting the parallel processes of self- and other-attention representation during interactions. However, direct evidence for the PDPM is limited due to a lack of ecologically valid experimental paradigms that can capture both RJA and IJA. Building on existing interactive approaches, we developed a virtual reality paradigm where participants engaged in an online interaction to complete a cooperative task. By including tightly controlled baseline conditions to remove activity associated with non-social task demands, we were able to directly contrast the neural correlates of RJA and IJA to determine whether these processes are supported by common brain regions. Both RJA and IJA activated broad frontotemporoparietal networks. Critically, a conjunction analysis identified that a subset of these regions were common to both RJA and IJA. This right-lateralised network included the dorsal portion of the middle frontal gyrus (MFG), inferior frontal gyrus (IFG), middle temporal gyrus (MTG), precentral gyrus, posterior superior temporal sulcus (pSTS), temporoparietal junction (TPJ) and precuneus. Additional activation was observed in this network for IJA relative to RJA at MFG, IFG, TPJ and precuneus. This is the first imaging study to directly investigate the neural correlates common to RJA and IJA engagement, and thus support the assumption that a broad integrated network underlies the parallel aspects of both initiating and responding to joint attention.

Beliefs about human agency influence the neural processing of gaze during joint attention

ABSTRACT The current study measured adults’ P350 and N170 ERPs while they interacted with a character in a virtual reality paradigm. Some participants believed the character was controlled by a human (“avatar” condition, n = 19); others believed it was controlled by a computer program (“agent” condition, n = 19). In each trial, participants initiated joint attention in order to direct the character’s gaze toward a target. In 50% of trials, the character gazed toward the target (congruent responses), and in 50% of trials the character gazed to a different location (incongruent response). In the avatar condition, the character’s incongruent gaze responses generated significantly larger P350 peaks at centro-parietal sites than congruent gaze responses. In the agent condition, the P350 effect was strikingly absent. Left occipitotemporal N170 responses were significantly smaller in the agent condition compared to the avatar condition for both congruent and incongruent gaze shifts. These data suggest that beliefs about human agency may recruit mechanisms that discriminate the social outcome of a gaze shift after approximately 350 ms, and that these mechanisms may modulate the early perceptual processing of gaze. These findings also suggest that the ecologically valid measurement of social cognition may depend upon paradigms that simulate genuine social interactions.

Detecting communicative intent in a computerised test of joint attention

The successful navigation of social interactions depends on a range of cognitive faculties—including the ability to achieve joint attention with others to share information and experiences. We investigated the influence that intention monitoring processes have on gaze-following response times during joint attention. We employed a virtual reality task in which 16 healthy adults engaged in a collaborative game with a virtual partner to locate a target in a visual array. In the Search task, the virtual partner was programmed to engage in non-communicative gaze shifts in search of the target, establish eye contact, and then display a communicative gaze shift to guide the participant to the target. In the NoSearch task, the virtual partner simply established eye contact and then made a single communicative gaze shift towards the target (i.e., there were no non-communicative gaze shifts in search of the target). Thus, only the Search task required participants to monitor their partner’s communicative intent before responding to joint attention bids. We found that gaze following was significantly slower in the Search task than the NoSearch task. However, the same effect on response times was not observed when participants completed non-social control versions of the Search and NoSearch tasks, in which the avatar’s gaze was replaced by arrow cues. These data demonstrate that the intention monitoring processes involved in differentiating communicative and non-communicative gaze shifts during the Search task had a measurable influence on subsequent joint attention behaviour. The empirical and methodological implications of these findings for the fields of autism and social neuroscience will be discussed.

Simulating social interactions for the experimental investigation of joint attention

HighlightsJoint attention should be investigated whilst participants are immersed in a social interaction.Virtual reality paradigms offer the optimal balance between validity and control.Interactions must be believable and realistically complex. ABSTRACT Social interactions are, by their nature, dynamic and reciprocal − your behaviour affects my behaviour, which affects your behaviour in return. However, until recently, the field of social cognitive neuroscience has been dominated by paradigms in which participants passively observe social stimuli from a detached “third person” perspective. Here we consider the unique conceptual and methodological challenges involved in adopting a “second person” approach whereby social cognitive mechanisms and their neural correlates are investigated within social interactions (Schilbach et al., 2013). The key question for researchers is how to distil a complex, intentional interaction between two individuals into a tightly controlled and replicable experimental paradigm. We explore these issues within the context of recent investigations of joint attention − the ability to coordinate a common focus of attention with another person. We review pioneering neurophysiology and eye‐tracking studies that have begun to address these issues; offer recommendations for the optimal design and implementation of interactive tasks, and discuss the broader implications of interactive approaches for social cognitive neuroscience.

Joint attention difficulties in autistic adults: An interactive eye-tracking study

Joint attention – the ability to coordinate attention with a social partner – is critical for social communication, learning and the regulation of interpersonal relationships. Infants and young children with autism demonstrate impairments in both initiating and responding to joint attention bids in naturalistic settings. However, little is known about joint attention abilities in adults with autism. Here, we tested 17 autistic adults and 17 age- and nonverbal intelligence quotient–matched controls using an interactive eye-tracking paradigm in which participants initiated and responded to joint attention bids with an on-screen avatar. Compared to control participants, autistic adults completed fewer trials successfully. They were also slower to respond to joint attention bids in the first block of testing but performed as well as controls in the second block. There were no group differences in responding to spatial cues on a non-social task with similar attention and oculomotor demands. These experimental results were mirrored in the subjective reports given by participants, with some commenting that they initially found it challenging to communicate using eye gaze, but were able to develop strategies that allowed them to achieve joint attention. Our study indicates that for many autistic individuals, subtle difficulties using eye-gaze information persist well into adulthood.

No association between autistic traits and contextual influences on eye-movements during reading.

Individuals with autism spectrum disorders are claimed to show a local cognitive bias, termed “weak central coherence”, which manifests in a reduced influence of contextual information on linguistic processing. Here, we investigated whether this bias might also be demonstrated by individuals who exhibit sub-clinical levels of autistic traits, as has been found for other aspects of autistic cognition. The eye-movements of 71 university students were monitored as they completed a reading comprehension task. Consistent with previous studies, participants made shorter fixations on words that were highly predicted on the basis of preceding sentence context. However, contrary to the weak central coherence account, this effect was not reduced amongst individuals with high levels of autistic traits, as measured by the Autism Spectrum Quotient (AQ). Further exploratory analyses revealed that participants with high AQ scores fixated longer on words that resolved the meaning of an earlier homograph. However, this was only the case for sentences where the two potential meanings of the homograph result in different pronunciations. The results provide tentative evidence for differences in reading style that are associated with autistic traits, but fail to support the notion of weak central coherence extending into the non-autistic population.

Human agency beliefs influence behaviour during virtual social interactions

In recent years, with the emergence of relatively inexpensive and accessible virtual reality technologies, it is now possible to deliver compelling and realistic simulations of human-to-human interaction. Neuroimaging studies have shown that, when participants believe they are interacting via a virtual interface with another human agent, they show different patterns of brain activity compared to when they know that their virtual partner is computer-controlled. The suggestion is that users adopt an “intentional stance” by attributing mental states to their virtual partner. However, it remains unclear how beliefs in the agency of a virtual partner influence participants’ behaviour and subjective experience of the interaction. We investigated this issue in the context of a cooperative “joint attention” game in which participants interacted via an eye tracker with a virtual onscreen partner, directing each other’s eye gaze to different screen locations. Half of the participants were correctly informed that their partner was controlled by a computer algorithm (“Computer” condition). The other half were misled into believing that the virtual character was controlled by a second participant in another room (“Human” condition). Those in the “Human” condition were slower to make eye contact with their partner and more likely to try and guide their partner before they had established mutual eye contact than participants in the “Computer” condition. They also responded more rapidly when their partner was guiding them, although the same effect was also found for a control condition in which they responded to an arrow cue. Results confirm the influence of human agency beliefs on behaviour in this virtual social interaction context. They further suggest that researchers and developers attempting to simulate social interactions should consider the impact of agency beliefs on user experience in other social contexts, and their effect on the achievement of the application’s goals.

The association between poor reading and internalising problems: A systematic review and meta-analysis

Numerous studies have demonstrated an association between learning disabilities and internalising problems such as anxiety and depression. However, our understanding of this association for people with specific types of learning disability - such as poor reading - is poorly understood. Here, we present the first systematic review and meta-analysis of studies that have examined associations between poor reading and internalising problems - including anxiety and depression - in children, adolescents, and adults. Our systematic search identified 34 studies comprising 16,275 participants (N = 2491 poor readers). Our meta-analysis revealed statistically significant differences between poor readers and typical readers on general measures of internalising problems (d = 0.41), as well as specific measures of anxiety (d = 0.41) and depression (d = 0.23). These outcomes suggest that poor readers are at moderate risk for experiencing internalising problems compared to typical readers, which appears to stem from a greater risk for anxiety than depression.