Background
Joint attention (JA) is important in early interaction as it is a fundamental aspect of interpersonal connection in typical social communicative development, underpinning referential understanding, shared concepts and perspective taking abilities (the ability to relate to others) as well as contributing to concordant inter-subjectivity [
1‐
3]. During typical infant-caregiver interactions, there is the ability to engage in order to share attention to objects or events of mutual interest and JA provides a context in which mutual regulation of affect and of problem solving, for the negotiation of communicative intentions and for the sharing of cultural meaning, can take place [
4,
5]. Active social behaviour increases dramatically around 1–2 months of age as infants begin to engage in direct face-to-face interactions with adults [
6‐
8]. Infant capacity for JA behaviours typically emerges between 6 and 12 months and involves the triadic interaction (‘jointness’) [
9] of attention between the infant, another person (typically an adult) and a third object such as a toy [
10‐
12]. JA is a term which characterises a wide range of behaviours including gaze and point following, showing and pointing. JA behaviours serve two different functions: imperative triadic exchanges serve an instrumental or requesting function, and declarative triadic exchanges which enables shared awareness or experience of an object or event [
13,
14].
The majority of research investigating JA surrounds its involvement in both cognitive and language development [
15,
16] while relatively little research has focused on the relationship of JA with social-emotional factors [
17]. JA skill development has been found to be involved in early adaptive social–emotional behavioural development [
18‐
20]. Since children who exhibit language development difficulties are at increased risk of behavioural and emotional disorders [
21‐
23], infant JA skills may be associated with both language development and social behavioural development. A number of JA behaviours in infancy are signs of processes associated with self-monitoring, emotional reactivity and prosocial affiliative tendencies [
24,
25] which are behavioural dimensions found to be associated with the emergence of social competence in young children [
26].
Recently, global characteristics of parent–infant interaction in 6–10 month-old at-risk and low-risk infants were examined using six minute videos of unstructured mother-infant play. At-risk infants were found to be less lively, and their parents exhibited both higher directiveness and lower sensitive responding [
27]. Marwick et al. [
28] recently demonstrated, using a holistic analysis of interpersonal behaviours within early social interaction, that lower levels of adult activity and adult speech predict later psychiatric diagnosis in the child at seven years of age. Analysis of the infants’ interactive behaviours revealed no predictors of later psychopathology.
Present study
Particular patterns of parent-infant interactions can aid prediction of later development of childhood psychopathology including attention deficit hyperactivity disorder (ADHD) and autism [
2]. JA abilities are crucially involved in the development of autism with impairments in JA amongst the earliest signs of the disorder [
29‐
36]. JA difficulties in relation to the external environment is argued to be an indicator or precursor for other adverse consequences in childhood: disruptive behaviour [
17,
37], disturbances in language development [
36] and disturbances in learning and social cognition [
38‐
40]. Disturbances in the parent–child relationship in early childhood are known risk factors for later psychological maladjustment [
41]. There is a need for examination of JA behaviours in adult-infant interaction to establish if these are predictive of later diagnosis of social communicative disorder to enable early identification and support. Identification of infant predictors of later childhood psychopathology is important for informing appropriate and timely intervention.
Based on videoed caregiver-infant interactions from a large population-based birth cohort, we examined whether analysis of mother-infant joint attention behaviours in social-communicative interaction at 12 months are predictive of later diagnosis of psychopathology in the child at seven years of age. To our knowledge, this is the first study which has examined whether mother-infant joint attention behaviours during an interaction when the infant is 12 months is predictive of later diagnosis of a wide range of psychopathologies, not simply autism, using a nested case–control study.
Results
Correlation between the raters was high for three of the four measures, consistent with high inter-rater reliability. Estimates of Kendall’s τ for shared look rate, shared attention rate and shared attention intensity were 0.83, 1.00 and 0.87, respectively, so these three measures were taken forward for further analysis. Kendall’s τ for “shared look (% time)” was low at 0.41, suggesting relatively poor reliability, and this measure was not analyzed further. There were no strong correlations between the three reliable measures (all |Spearman’s ρ| < 0.5), suggesting low redundancy. Summary statistics for the three reliable joint attention measures are presented in Table
2.
Table 2
Summary statistics for the three reliable joint attention measures in controls and cases
Shared look rate (count/min) | Mean (SD) | 0.21 (0.42) | 0.25 (0.34) |
Median (IQR) | 0.00 (0.00, 0.21) | 0.00 (0.00, 0.48) |
[Range] | [0.00, 2.32] | [0.00, 1.35] |
Shared attention rate (count/min) | Mean (SD) | 3.1 (1.3) | 3.0 (1.6) |
Median (IQR) | 3.1 (2.2, 3.7) | 2.9 (1.9, 4.1) |
[Range] | [0.0, 7.7] | [0.0, 6.7] |
Shared attention intensity (% time) | Mean (SD) | 67 (16) | 66 (21) |
Median (IQR) | 69 (60, 79) | 69 (59, 80) |
[Range] | [0, 95] | [0, 94] |
Of the potential confounders, maternal depression, an infant having a father with a “manual” occupation and maternal age were associated with measures of JA. Depression scores tended to be negatively associated, or nearly so, with shared look rate (
p = 0.332 at 32–40 weeks gestation;
p = 0.052 at eight months postnatal) and shared attention rate (
p = 0.033 at 32–40 weeks gestation;
p = 0.093 at 8 months postnatal), but positively associated with shared attention intensity (
p = 0.002 at 32–40 weeks gestation;
p = 0.030 at eight months postnatal). EPDS depression scores are summarised and compared between the case–control groups in Table
3.
Table 3
Mean (SD) Edinburgh Postnatal Depression Scale (EPDS) scores at 32–40 weeks gestation and 8 months postnatal among controls and cases
32-40 weeks gestationb
| 5.9 (4.0) | 8.7 (6.1) | 0.004 |
8 months postnatal | 5.0 (4.6) | 6.9 (5.7) | 0.038 |
Mean of 32–40 weeks gestation and 8 months postnatal | 5.4 (3.7) | 7.8 (5.3) | 0.005 |
Because these two depression scores were strongly positively correlated with each other (Spearman’s ρ = 0.59), and neither showed a consistently stronger association than the other with the shared attention measures, we combined these into a single mean depression score, which was consistently significantly associated with all three joint attention measures (all p < 0.05). All subsequent models were adjusted for this mean depression score.
In addition, having a father with a “manual” occupation was negatively associated with shared attention rate (
p = 0.073), maternal age was negatively associated with shared attention intensity (
p = 0.078), and log interaction duration was positively associated with shared attention intensity (
p = 0.075). Models predicting shared attention rate were therefore additionally adjusted for paternal occupation, while models predicting shared attention intensity were additionally adjusted for maternal age and log video duration, respectively. However, adjusting for these potential confounders had no substantial effect on the results presented in Table
4.
Table 4
Logistic regression analyses showing odds ratios (OR) with 95% confidence intervals (CI) and p-values relative to controls (n = 106) between joint attention measures and case–control status, including overall case status and diagnostic subgroups
All cases | 53 | 1.2 (0.9, 1.7) | 1.0 (0.7, 1.5) | 0.8 (0.6, 1.2) |
p = 0.269 | p = 0.892 | p = 0.329 |
Diagnostic subgroup | | | | |
| Disruptive behaviour disorders (any ADHD + any oppositional-conduct disorder) | 32 | 1.3 (0.9, 1.9) p = 0.156 | 1.0 (0.7, 1.6) p = 0.900 | 0.7 (0.5, 1.1) p = 0.132 |
| Any ADHD disorder | 15 | 1.1 (0.6, 1.7) p = 0.719 | 0.9 (0.5, 1.6) p = 0.820 | 0.6 (0.4, 1.1) p = 0.095 |
| Any oppositional-conduct disorder | 24 | 1.5 (1.0, 2.3) p = 0.041 | 1.1 (0.7, 1.8) p = 0.699 | 0.8 (0.5, 1.2) p = 0.259 |
| Pervasive development disorder | 5 | 1.2 (0.4, 2.0) p = 0.655 | 0.6 (0.2, 1.6) p = 0.328 | 1.6 (0.5, 6.9) p = 0.438 |
| Any emotional disorder | 24 | 1.3 (0.8, 1.9) p = 0.217 | 1.2 (0.7, 2.2) p = 0.495 | 0.9 (0.5, 1.7) p = 0.761 |
None of the three joint attention measures showed a significant association with the primary outcome of case–control status (Table
4). Only shared look rate predicted any of the exploratory sub-diagnosis outcomes, being positively associated with diagnosis of any oppositional-conduct disorder (
p = 0.041). A positive difference of one SD in the shared look rate (equivalent to an additional two shared looks every five minutes; Table
2) predicted an approximately 50% increase (OR [95% CI]: 1.5 [1.0, 2.3]) in the odds of diagnosis with any oppositional-conduct disorder (Table
4). An alternative way of viewing this association is that subjects diagnosed with any oppositional-conduct disorder shared looks with their caregiver more frequently, on average, than did controls (mean looks/min in cases: 0.35; controls: 0.21).
Discussion
Based on a large cohort of infants, we investigated whether it was possible to predict diagnosis of psychiatric disorders from analysis of mother-infant joint attention behaviours in social-communicative interaction at 12 months.
Specifically, we examined three JA behaviours: shared look rate (count/min), shared attention rate (count/min)
and shared attention intensity (% time). There was no evidence that JA at one year strongly predicts psychopathology at age seven. None of the three JA measures showed a significant association with the primary outcome of case–control status. Only shared look rate predicted any of the exploratory sub-diagnosis outcomes and was found to be positively associated with later oppositional-conduct disorders.
It is possible that other associations exist but were not detected in this study. There are a variety of explanations for this. Firstly, the methodological shortcomings of our study need to be considered. Our study was powered to detect only strong effects which was something that we could not modify in this exploratory study. With regards to the sub-diagnoses, some of these had very small sample sizes, so associations would have had to be very strong indeed to have been detected. Potential existence of weaker associations, not detectable by the present exploratory study, may be due to the case group being too broadly defined, so that true associations between JA measures and sub-diagnoses might be hidden due to being combined in the case group with diagnoses with no association or opposite associations. However, this explanation is not well supported by the results of the tests for association between the three joint attention measures and the five sub-diagnoses, since only one of the 15 tests – between the rate of shared looks and any oppositional-conduct disorder – was significant, which is close to the number expected due to chance alone.
The angle of the camera recording the videos is a potential limitation as discussed earlier in the methods section. Additionally, it is possible that the structure of the book situation (caregiver asked to share a picture book with their infant and engage their child in this activity as they would at home) reduced the social demand of the context and modulated the child’s activity and behaviour masking possible associations between JA behaviours and later diagnosis. Therefore, the scaffolding measures adopted during the task by the caregiver is creating a more controlled and limiting environment than say a free play situation. Nevertheless, the observers were able to assess variation in JA levels between videos, and do this with high inter-rater reliability. However, it may simply be the case that there really are no other associations or significant predictors of later diagnoses observable from the JA behaviours and the single significant result was due to chance. There is also the issue of accuracy of the DAWBA version which was used in identifying psychopathology in the present study. It has been considered limited in its ability to identify autism – the five cases of PDD were not identified as having an ASD by the clinicians. The PDD diagnoses were not made using the specific section of the DAWBA which was developed later, instead the diagnoses were made incidentally from other questions. In sum, we found no evidence that JA at one year strongly predicts psychopathology as a whole at age seven.
From previous literature, it is possible that the reason no association was found between JA and psychopathology in the present early sample is that psychiatric disorders, including ADHD, have been found to take different trajectories from infancy to adolescence [
50,
51]. Shared attention also failed to predict autism (one of the five types of pervasive developmental disorders) which may be due to the caregiver compensating for the infant’s behaviour [
52]. Previous studies have found shared attention or JA difficulties in infancy [
30] and it is even argued to be one of the earliest signs of autism [
31,
32]. The small sample size of only five cases may be a reason for the lack of significant findings with respect to the prediction of later diagnosis of pervasive development disorder. It is also possible that joint attention between caregivers and infants can neither explain nor predict later psychopathology, so that the association between shared look rate and any oppositional-conduct disorder was a chance result. Additionally, there may be cases within the control group and vice versa [
52,
53], since both under-diagnosis and over-diagnosis routinely occur in ADHD [
54,
55]. Surprisingly our study found that, of the three joint attention behaviours, only shared look was positively associated with later oppositional-conduct disorders and none of the joint attention behaviours predicted or were associated with ADHD. A potential interpretation of this finding is that the mothers of the infants later diagnosed with ADHD were perhaps (even on an unconscious level) controlling the infants impulsivity and “watching” the infants behaviour. It may also be an indication of extroversion in both the mother and infant or infant alone. Previous research however has shown in
older children aged between 4–8 years that, compared with controls, children with oppositional defiant disorder expressed lower levels of affection back towards their mothers; those with high levels of callous-unemotional traits showed significantly lower levels of affection than the children lacking these traits. The former group exhibited lower levels of eye contact toward their mothers. These impairments were found to be independent of maternal behaviour. No group difference in affection and eye contact expressed by the mothers was found [
49].
We have presented a case–control study nested within a prospective longitudinal cohort study. The longitudinal nature of the study is one of its main strengths. Previous studies have either been retrospective or have sampled high risk referred children or siblings of affected individuals. Retrospective studies are limited in that they are primarily based on parental reports which are often biased and subject to recall/memory problems. Here we report the first study of the utility of measures of joint attention in early mother-infant interaction in predicting later onset of childhood psychopathology, based on a large cohort of infants from the ALSPAC community-based cohort. Another important strength of the present study is that all the children in the study received an independent psychiatric assessment at age seven years using the DAWBA [
44]. Lastly, we made a partial adjustment for caregiver psychopathology via the maternal depression rating which is important to strengthen the conclusions we draw from our findings given that there is much evidence strongly indicating the impact of maternal psychopathology on infant cognitive and psychological development [
56,
57] and behaviour [
58]. On the other hand, one study found that maternal depression (whether prior to the birth, postpartum, or at nine months) had little impact on JA between a caregiver and nine month old infants and therefore, relationships between JA and maternal behaviour reflect infants’ social interactions with their mothers, not depression
per se[
59,
60].
A future study could also improve the quality of video recording to ensure that parent and child faces are always in optimum view. A new larger cohort, comprising ‘at-risk’ infants using more task conditions (i.e. play, feed, etc.), could be implemented using a placement of video equipment which would enable the capturing of more information. These more naturalistic settings might reveal more than the constrained setting of TIM and a previous study has found it to be an effective method [
61]. It remains to be established whether analyses of this kind can contribute to the development of screening instruments for disorders amenable to early intervention [
61].
Acknowledgements
We are extremely grateful to all the families who took part in this study, the midwives for their help in recruiting them, and the whole ALSPAC team, which includes interviewers, computer and laboratory technicians, clerical workers, research scientists, volunteers, managers, receptionists, and nurses. The United Kingdom Medical Research Council, the Wellcome Trust (grant ref: 092731) and the University of Bristol currently provide core support for ALSPAC. The project was specifically funded by small grants from the Yorkhill Children’s Foundation, the Gillberg Neuropsychiatry Centre and the Waterloo Foundation. This article is the work of the authors, and Philip Wilson will serve as guarantor for the contents of this article.
Competing interests
The authors declare no conflicts of interests.
Authors’ contributions
CSA drafted the manuscript with PJ. PJ performed the statistical analysis under AM's supervision. CP, EL and EK supervised the observations. AM; HM; JG; CP and CG designed the study. PW designed study and is the principal investigator and guarantor for the contents of this article. All ten authors reviewed the manuscript.
Financial competing interests
ALSPAC currently receives core support from Wellcome Trust, Medical Research Council and the University of Bristol. This project was specifically funded by small grants from the Yorkhill Children’s Foundation, the Gillberg Neuropsychiatry Centre and the Waterloo Foundation.
Non-financial competing interests
The authors declare no non-financial competing interests.