The roles of sensory hyperreactivity and hyporeactivity in understanding infant fearfulness and emerging autistic traits.

Autism anxiety early development elevated likelihood hyperreactivity hyporeactivity sensory reactivity

Journal

Journal of child psychology and psychiatry, and allied disciplines
ISSN: 1469-7610
Titre abrégé: J Child Psychol Psychiatry
Pays: England
ID NLM: 0375361

Informations de publication

Date de publication:
03 Jan 2024
Historique:
accepted: 31 10 2023
medline: 4 1 2024
pubmed: 4 1 2024
entrez: 3 1 2024
Statut: aheadofprint

Résumé

Existing evidence indicates that atypical sensory reactivity is a core characteristic of autism, and has been linked to both anxiety (and its putative infant precursor of fearfulness) and repetitive behaviours. However, most work has used cross-sectional designs and not considered the differential roles of hyperreactivity and hyporeactivity to sensory inputs, and is thus limited in specificity. 161 infants with and without an elevated likelihood of developing autism and attention-deficit hyperactivity disorder (ADHD) were followed from 10 to 36 months of age. Parents rated an infant precursor of later anxiety (fearfulness) using the Infant Behaviour Questionnaire at 10 and 14 months, and the Early Childhood Behavioural Questionnaire at 24 months, and sensory hyperreactivity and hyporeactivity at 10, 14 and 24 months using the Infant Toddler Sensory Profile. Domains of autistic traits (restrictive and repetitive behaviours; RRB, and social communication interaction, SCI) were assessed using the parent-rated Social Responsiveness Scale at 36 months. Cross-lagged models tested (a) paths between fearfulness and hyperreactivity at 10-24 months, and from fearfulness and hyperreactivity to later autism traits, (b) the specificity of hyperreactivity effects by including hyporeactivity as a correlated predictor. Hyperreactivity at 14 months was positively associated with fearfulness at 24 months, and hyperreactivity at 24 months was positively associated with SCI and RRB at 36 months. When hyporeactivity was included in the model, paths between hyperreactivity and fearfulness remained, but paths between hyperreactivity and autistic traits became nonsignificant. Our findings indicate that alterations in early sensory reactivity may increase the likelihood of showing fearfulness in infancy, and relate to later social interactions and repetitive behaviours, particularly in individuals with a family history of autism or ADHD.

Sections du résumé

BACKGROUND BACKGROUND
Existing evidence indicates that atypical sensory reactivity is a core characteristic of autism, and has been linked to both anxiety (and its putative infant precursor of fearfulness) and repetitive behaviours. However, most work has used cross-sectional designs and not considered the differential roles of hyperreactivity and hyporeactivity to sensory inputs, and is thus limited in specificity.
METHODS METHODS
161 infants with and without an elevated likelihood of developing autism and attention-deficit hyperactivity disorder (ADHD) were followed from 10 to 36 months of age. Parents rated an infant precursor of later anxiety (fearfulness) using the Infant Behaviour Questionnaire at 10 and 14 months, and the Early Childhood Behavioural Questionnaire at 24 months, and sensory hyperreactivity and hyporeactivity at 10, 14 and 24 months using the Infant Toddler Sensory Profile. Domains of autistic traits (restrictive and repetitive behaviours; RRB, and social communication interaction, SCI) were assessed using the parent-rated Social Responsiveness Scale at 36 months. Cross-lagged models tested (a) paths between fearfulness and hyperreactivity at 10-24 months, and from fearfulness and hyperreactivity to later autism traits, (b) the specificity of hyperreactivity effects by including hyporeactivity as a correlated predictor.
RESULTS RESULTS
Hyperreactivity at 14 months was positively associated with fearfulness at 24 months, and hyperreactivity at 24 months was positively associated with SCI and RRB at 36 months. When hyporeactivity was included in the model, paths between hyperreactivity and fearfulness remained, but paths between hyperreactivity and autistic traits became nonsignificant.
CONCLUSIONS CONCLUSIONS
Our findings indicate that alterations in early sensory reactivity may increase the likelihood of showing fearfulness in infancy, and relate to later social interactions and repetitive behaviours, particularly in individuals with a family history of autism or ADHD.

Identifiants

pubmed: 38172076
doi: 10.1111/jcpp.13941
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Maudsley Charity
ID : 980
Organisme : EFPIA and AUTISM SPEAKS, Autistica, SFARI
Organisme : Medical Research Council Centre for Neurodevelopmental Disorders
ID : MR/K021389/1
Organisme : Medical Research Council Centre for Neurodevelopmental Disorders
ID : MR/T003057/1
Organisme : Henry Wellcome Postdoctoral Fellowship
ID : 213608/Z/18/Z
Organisme : Innovative Medicines Initiative 2 Joint Undertaking
ID : 777394
Organisme : European Union's Horizon 2020 research and innovation programme
Organisme : Guy's and St Thomas' Charity
ID : STR130505

Investigateurs

Mary Agyapong (M)
Tessel Bazelmans (T)
Leila Dafner (L)
Mutluhan Ersoy (M)
Teodora Gliga (T)
Amy Goodwin (A)
Rianne Haartsen (R)
Hanna Halkola (H)
Alexandra Hendry (A)
Rebecca Holman (R)
Sarah Kalwarowsky (S)
Anna Kolesnik (A)
Leyan Li (L)
Luke Mason (L)
Chloë Taylor (C)

Informations de copyright

© 2024 The Authors. Journal of Child Psychology and Psychiatry published by John Wiley & Sons Ltd on behalf of Association for Child and Adolescent Mental Health.

Références

American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (DSM-5).
Antshel, K.M., & Russo, N. (2019). Autism spectrum disorders and ADHD: Overlapping phenomenology, diagnostic issues, and treatment considerations. Current Psychiatry Reports, 21, 34.
Asendorpf, J.B., Conner, M., De Fruyt, F., De Houwer, J., Denissen, J.J., Fiedler, K., … & Nosek, B.A. (2016). Recommendations for increasing replicability in psychology.
Baranek, G.T., Watson, L.R., Boyd, B.A., Poe, M.D., David, F.J., & McGuire, L. (2013). Hyporesponsiveness to social and nonsocial sensory stimuli in children with autism, children with developmental delays, and typically developing children. Development and Psychopathology, 25, 307-320.
Baranek, G.T., Woynaroski, T.G., Nowell, S., Turner-Brown, L., DuBay, M., Crais, E.R., & Watson, L.R. (2018). Cascading effects of attention disengagement and sensory seeking on social symptoms in a community sample of infants at-risk for a future diagnosis of autism spectrum disorder. Developmental Cognitive Neuroscience, 29, 30-40.
Begum-Ali, J., Goodwin, A., Mason, L., Pasco, G., Charman, T., Johnson, M.H., … & Team, T.S. (2022). Altered theta-beta ratio in infancy associates with family history of ADHD and later ADHD-relevant temperamental traits. Journal of Child Psychology and Psychiatry, 63, 1057-1067.
Black, K.R., Stevenson, R.A., Segers, M., Ncube, B.L., Sun, S.Z., Philipp-Muller, A., … & Ferber, S. (2017). Linking anxiety and insistence on sameness in autistic children: The role of sensory hypersensitivity. Journal of Autism and Developmental Disorders, 47, 2459-2470.
Boyd, B.A., Baranek, G.T., Sideris, J., Poe, M.D., Watson, L.R., Patten, E., & Miller, H. (2010). Sensory features and repetitive behaviors in children with autism and developmental delays. Autism Research, 3, 78-87.
Bradshaw, J., Schwichtenberg, A.J., & Iverson, J.M. (2022). Capturing the complexity of autism: Applying a developmental cascades framework. Child Development Perspectives, 16, 18-26.
Carpenter, K.L., Baranek, G.T., Copeland, W.E., Compton, S., Zucker, N., Dawson, G., & Egger, H.L. (2019). Sensory over-responsivity: An early risk factor for anxiety and behavioral challenges in young children. Journal of Abnormal Child Psychology, 47, 1075-1088.
Chen, Y.J., Sideris, J., Watson, L.R., Crais, E.R., & Baranek, G.T. (2022). Developmental trajectories of sensory patterns from infancy to school age in a community sample and associations with autistic traits. Child Development, 93, e446-e459.
Constantino, J., & Gruber, C.P. (2012). Social responsiveness scale: SRS-2. Torrance, CA: Western Psychological Services.
Crane, L., Goddard, L., & Pring, L. (2009). Sensory processing in adults with autism spectrum disorders. Autism, 13, 215-228.
Dunn, W. (2002). The infant toddler sensory profile. San Antonio, TX: Psychological Corporation.
Elwin, M., Ek, L., Kjellin, L., & Schröder, A. (2013). Too much or too little: Hyper-and hypo-reactivity in high-functioning autism spectrum conditions. Journal of Intellectual & Developmental Disability, 38, 232-241.
Ersoy, M., Charman, T., Pasco, G., Carr, E., Johnson, M.H., & Jones, E.J. (2021). Developmental paths to anxiety in an autism-enriched infant cohort: The role of temperamental reactivity and regulation. Journal of Autism and Developmental Disorders, 51, 2631-2645.
Feldman, J.I., Raj, S., Bowman, S.M., Santapuram, P., Golden, A.J., Daly, C., … & Woynaroski, T.G. (2021). Sensory responsiveness is linked with communication in infant siblings of children with and without autism. Journal of Speech, Language, and Hearing Research, 64, 1964-1976.
Gartstein, M., Bridgett, D.J., Rothbart, M.K., Robertson, C., Iddins, E., Ramsay, K., & Schlect, S. (2010). A latent growth examination of fear development in infancy: Contributions of maternal depression and the risk for toddler anxiety. Developmental Psychology, 46, 651-668.
Gartstein, M., & Rothbart, M.K. (2003). Studying infant temperament via the revised infant behavior questionnaire. Infant Behavior and Development, 26, 64-86.
Germani, T., Zwaigenbaum, L., Bryson, S., Brian, J., Smith, I., Roberts, W., … & Vaillancourt, T. (2014). Brief report: Assessment of early sensory processing in infants at high-risk of autism spectrum disorder. Journal of Autism and Developmental Disorders, 44, 3264-3270.
Gotham, K., Bishop, S.L., Hus, V., Huerta, M., Lund, S., Buja, A., … & Lord, C. (2013). Exploring the relationship between anxiety and insistence on sameness in autism spectrum disorders. Autism Research, 6, 33-41.
Green, S.A., Ben-Sasson, A., Soto, T.W., & Carter, A.S. (2012). Anxiety and sensory over-responsivity in toddlers with autism spectrum disorders: Bidirectional effects across time. Journal of Autism and Developmental Disorders, 42, 1112-1119.
Grzadzinski, R., Di Martino, A., Brady, E., Mairena, M.A., O'Neale, M., Petkova, E., … & Castellanos, F.X. (2011). Examining autistic traits in children with ADHD: Does the autism spectrum extend to ADHD? Journal of Autism and Developmental Disorders, 41, 1178-1191.
Grzadzinski, R., Donovan, K., Truong, K., Nowell, S., Lee, H., Sideris, J., … & Watson, L.R. (2020). Sensory reactivity at 1 and 2 years old is associated with ASD severity during the preschool years. Journal of Autism and Developmental Disorders, 50, 3895-3904.
Hamaker, E.L., Kuiper, R.M., & Grasman, R.P. (2015). A critique of the cross-lagged panel model. Psychological Methods, 20, 102-116.
Havdahl, K.A., Hus Bal, V., Huerta, M., Pickles, A., Øyen, A.-S., Stoltenberg, C., … & Bishop, S.L. (2016). Multidimensional influences on autism symptom measures: Implications for use in etiological research. Journal of the American Academy of Child & Adolescent Psychiatry, 55, 1054-1063.e1053.
He, J., Williams, Z., Harris, A., Powell, H., Schaaf, R., Tavassoli, T., & Puts, N. (2022). Working taxonomy for describing the sensory differences of autism. PsyArXiv. https://doi.org/10.31234/osf.io/jmv6k
Jones, E.J., Dawson, G., & Webb, S. (2018). Sensory hypersensitivity predicts enhanced attention capture by faces in the early development of ASD. Developmental Cognitive Neuroscience, 29, 11-20.
Kapp, S.K., Steward, R., Crane, L., Elliott, D., Elphick, C., Pellicano, E., & Russell, G. (2019). ‘People should be allowed to do what they like’: Autistic adults' views and experiences of stimming. Autism, 23, 1782-1792.
Kirby, A.V., Bilder, D.A., Wiggins, L.D., Hughes, M.M., Davis, J., Hall-Lande, J.A., … & Bakian, A.V. (2022). Sensory features in autism: Findings from a large population-based surveillance system. Autism Research, 15, 751-760.
Lidstone, J., Uljarevic, M., Sullivan, J., Rodgers, J., McConachie, H., Freeston, M., … & Leekam, S. (2014). Relations among restricted and repetitive behaviors, anxiety and sensory features in children with autism spectrum disorders. Research in Autism Spectrum Disorders, 8, 82-92.
Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., & Bishop, S. (2012). (ADOS®-2) autism diagnostic observation schedule™ Second edition. (ADOS®-2) Autism Diagnostic Observation Schedule.
Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism diagnostic interview-revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659-685.
Marco, E.J., Khatibi, K., Hill, S.S., Siegel, B., Arroyo, M.S., Dowling, A.F., … & Nagarajan, S.S. (2012). Children with autism show reduced somatosensory response: An MEG study. Autism Research, 5, 340-351.
McCulloch, C.E., Lin, H., Slate, E.H., & Turnbull, B.W. (2002). Discovering subpopulation structure with latent class mixed models. Statistics in Medicine, 21, 417-429.
Mullen, E.M. (1995). Mullen scales of early learning. Circle Pines, MN: AGS.
Mund, M., & Nestler, S. (2019). Beyond the cross-lagged panel model: Next-generation statistical tools for analyzing interdependencies across the life course. Advances in Life Course Research, 41, 100249.
Narvekar, N., Carter Leno, V., Pasco, G., Johnson, M.H., Jones, E.J., & Charman, T. (2022). A prospective study of associations between early fearfulness and perceptual sensitivity and later restricted and repetitive behaviours in infants with typical and elevated likelihood of autism. Autism, 26, 1947-1958.
Niedźwiecka, A., Domasiewicz, Z., Kawa, R., Tomalski, P., & Pisula, E. (2019). Sensory processing in toddlers with autism spectrum disorders. European Journal of Developmental Psychology, 17, 527-555.
Nijmeijer, J.S., Minderaa, R.B., Buitelaar, J.K., Mulligan, A., Hartman, C.A., & Hoekstra, P.J. (2008). Attention-deficit/hyperactivity disorder and social dysfunctioning. Clinical Psychology Review, 28, 692-708.
Nosek, B.A., Hardwicke, T.E., Moshontz, H., Allard, A., Corker, K.S., Dreber, A., … & Nuijten, M.B. (2022). Replicability, robustness, and reproducibility in psychological science. Annual Review of Psychology, 73, 719-748.
Nowell, S.W., Watson, L.R., Crais, E.R., Baranek, G.T., Faldowski, R.A., & Turner-Brown, L. (2020). Joint attention and sensory-regulatory features at 13 and 22 months as predictors of preschool language and social-communication outcomes. Journal of Speech, Language, and Hearing Research, 63, 3100-3116.
Posar, A., & Visconti, P. (2018). Sensory abnormalities in children with autism spectrum disorder. Jornal de Pediatria, 94, 342-350.
Putnam, S.P., Gartstein, M., & Rothbart, M.K. (2006). Measurement of fine-grained aspects of toddler temperament: The early childhood behavior questionnaire. Infant Behavior and Development, 29, 386-401.
Rodgers, J., Glod, M., Connolly, B., & McConachie, H. (2012). The relationship between anxiety and repetitive behaviours in autism spectrum disorder. Journal of Autism and Developmental Disorders, 42, 2404-2409.
Ronald, A., Larsson, H., Anckarsäter, H., & Lichtenstein, P. (2014). Symptoms of autism and ADHD: A Swedish twin study examining their overlap. Journal of Abnormal Psychology, 123, 440-451.
Ronald, A., Simonoff, E., Kuntsi, J., Asherson, P., & Plomin, R. (2008). Evidence for overlapping genetic influences on autistic and ADHD behaviours in a community twin sample. Journal of Child Psychology and Psychiatry, 49, 535-542.
Sacrey, L.-A.R., Zwaigenbaum, L., Bryson, S., Brian, J., Smith, I.M., Roberts, W., … & Novak, C. (2015). Can parents' concerns predict autism spectrum disorder? A prospective study of high-risk siblings from 6 to 36 months of age. Journal of the American Academy of Child & Adolescent Psychiatry, 54, 470-478.
Scheerer, N.E., Pourtousi, A., Yang, C., Ding, Z., Stojanoski, B., Anagnostou, E., … & Stevenson, R.A. (2022). Transdiagnostic patterns of sensory processing in autism and ADHD. Journal of Autism and Developmental Disorders, 1-13. https://doi.org/10.1007/s10803-022-05798-3
Schulz, S., Kelley, E., Anagnostou, E., Nicolson, R., Georgiades, S., Crosbie, J., … & Stevenson, R.A. (2023). Sensory processing patterns predict problem behaviours in autism spectrum disorder and attention-deficit/hyperactivity disorder. Advances in Neurodevelopmental Disorders, 7, 46-58.
Schulz, S., & Stevenson, R.A. (2019). Differentiating between sensory sensitivity and sensory reactivity in relation to restricted interests and repetitive behaviours. Autism, 24, 121-134.
Schwarzlose, R.F., Tillman, R., Hoyniak, C.P., Luby, J.L., & Barch, D.M. (2022). Sensory over-responsivity: A feature of childhood psychiatric illness associated with altered functional connectivity of sensory networks. Biological Psychiatry, 93, 92-101.
Shen, M.D., & Piven, J. (2022). Brain and behavior development in autism from birth through infancy. Dialogues in Clinical Neuroscience, 19, 325-333.
Shephard, E., Bedford, R., Milosavljevic, B., Gliga, T., Jones, E.J.H., Pickles, A., … & Charman, T. (2019). Early developmental pathways to childhood symptoms of attention-deficit hyperactivity disorder, anxiety and autism spectrum disorder. Journal of Child Psychology and Psychiatry, 60, 963-974.
Shephard, E., Zuccolo, P.F., Idrees, I., Godoy, P.B.G., Salomone, E., Ferrante, C., … & Polanczyk, G.V. (2022). Systematic review and meta-analysis: The science of early-life precursors and interventions for attention-deficit/hyperactivity disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 61, 187-226.
Sparrow, S., Cicchetti, D., & Balla, D.A. (2005). Vineland adaptive behavior scales second edition survey forms manual. Circle Pines, MN: America Guidance Service.
Tavassoli, T., Brandes-Aitken, A., Chu, R., Porter, L., Schoen, S., Miller, L.J., … & Marco, E.J. (2019). Sensory over-responsivity: Parent report, direct assessment measures, and neural architecture. Molecular Autism, 10, 1-10.
Tillmann, J., Uljarevic, M., Crawley, D., Dumas, G., Loth, E., Murphy, D., … & Charman, T. (2020). Dissecting the phenotypic heterogeneity in sensory features in autism spectrum disorder: A factor mixture modelling approach. Molecular Autism, 11, 67.
Tomlinson, P.S., Harbaugh, B.L., & Anderson, K. (1996). Children's temperament at 3 months and 6 years old: Stability, reliability, and measurement issues. Issues in Comprehensive Pediatric Nursing, 19, 33-47.
Tonnsen, B.L., Malone, P.S., Hatton, D.D., & Roberts, J.E. (2013). Early negative affect predicts anxiety, not autism, in preschool boys with fragile X syndrome. Journal of Abnormal Child Psychology, 41, 267-280.
Vlaeminck, F., Vermeirsch, J., Verhaeghe, L., Warreyn, P., & Roeyers, H. (2020). Predicting cognitive development and early symptoms of autism spectrum disorder in preterm children: The value of temperament and sensory processing. Infant Behavior & Development, 59, 101442.
Wigham, S., Rodgers, J., South, M., McConachie, H., & Freeston, M. (2015). The interplay between sensory processing abnormalities, intolerance of uncertainty, anxiety and restricted and repetitive behaviours in autism spectrum disorder. Journal of Autism and Developmental Disorders, 45, 943-952.
Williams, K.L., Campi, E., & Baranek, G.T. (2021). Associations among sensory hyperresponsiveness, restricted and repetitive behaviors, and anxiety in autism: An integrated systematic review. Research in Autism Spectrum Disorders, 83, 101763.
Wolff, J.J., Dimian, A.F., Botteron, K.N., Dager, S.R., Elison, J.T., Estes, A.M., … & Network, I. (2019). A longitudinal study of parent-reported sensory responsiveness in toddlers at-risk for autism. Journal of Child Psychology and Psychiatry, 60, 314-324.

Auteurs

Nisha Narvekar (N)

Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Virginia Carter Leno (V)

Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Greg Pasco (G)

Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Jannath Begum Ali (J)

Centre for Brain and Cognitive Development, Birkbeck, London, UK.

Mark H Johnson (MH)

Centre for Brain and Cognitive Development, Birkbeck, London, UK.
Department of Psychology, University of Cambridge, Cambridge, UK.

Tony Charman (T)

Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Emily J H Jones (EJH)

Centre for Brain and Cognitive Development, Birkbeck, London, UK.

Classifications MeSH