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. 2021 Jan 4;13(1):1.
doi: 10.1186/s11689-020-09334-1.

Behavioural and neural markers of tactile sensory processing in infants at elevated likelihood of autism spectrum disorder and/or attention deficit hyperactivity disorder

Elena Serena Piccardi  1 , Jannath Begum Ali  2 , Emily J H Jones  2 , Luke Mason  2 , Tony Charman  3 , Mark H Johnson  2   4 , Teodora Gliga  2   5 ; BASIS/STAARS Team
Collaborators, Affiliations

Behavioural and neural markers of tactile sensory processing in infants at elevated likelihood of autism spectrum disorder and/or attention deficit hyperactivity disorder

Elena Serena Piccardi et al. J Neurodev Disord. .

Abstract

Backgrounds: Atypicalities in tactile processing are reported in autism spectrum disorder (ASD) and attention deficit hyperactivity disorder (ADHD) but it remains unknown if they precede and associate with the traits of these disorders emerging in childhood. We investigated behavioural and neural markers of tactile sensory processing in infants at elevated likelihood of ASD and/or ADHD compared to infants at typical likelihood of the disorders. Further, we assessed the specificity of associations between infant markers and later ASD or ADHD traits.

Methods: Ninety-one 10-month-old infants participated in the study (n = 44 infants at elevated likelihood of ASD; n = 20 infants at elevated likelihood of ADHD; n = 9 infants at elevated likelihood of ASD and ADHD; n = 18 infants at typical likelihood of the disorders). Behavioural and EEG responses to pairs of tactile stimuli were experimentally recorded and concurrent parental reports of tactile responsiveness were collected. ASD and ADHD traits were measured at 24 months through standardized assessment (ADOS-2) and parental report (ECBQ), respectively.

Results: There was no effect of infants' likelihood status on behavioural markers of tactile sensory processing. Conversely, increased ASD likelihood associated with reduced neural repetition suppression to tactile input. Reduced neural repetition suppression at 10 months significantly predicted ASD (but not ADHD) traits at 24 months across the entire sample. Elevated tactile sensory seeking at 10 months moderated the relationship between early reduced neural repetition suppression and later ASD traits.

Conclusions: Reduced tactile neural repetition suppression is an early marker of later ASD traits in infants at elevated likelihood of ASD or ADHD, suggesting that a common pathway to later ASD traits exists despite different familial backgrounds. Elevated tactile sensory seeking may act as a protective factor, mitigating the relationship between early tactile neural repetition suppression and later ASD traits.

Keywords: Alpha amplitude desynchronization; Attention deficit hyperactivity disorder; Autism spectrum disorder; EEG; Infant sibling design; Repetition suppression; Tactile sensory processing; Tactile sensory seeking.

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Conflict of interest statement

The authors declare that they have no competing interests

Figures

Fig. 1
Fig. 1
a Representation of the sequence of events in the tactile repetition suppression paradigm. Pairs of 200-ms-long vibrotactile stimuli were delivered to the infants’ feet with a 700-ms ISI within the pair and 8–12 s ISI between the pairs. Pre-stimulus and post-stimulus phases (4 s each) are highlighted in yellow. b High-density EEG was recorded while vibrotactile stimuli were delivered to the infants’ feet through custom-made tactors (the light blue circle indicates the location of one tactor). c Hydrocel-Geodesic Sensor Net montage displaying the central somatosensory pool of electrodes (black circle) used for quantifying α desynchronization (6–10 Hz) to vibrotactile stimulation. The pool corresponded spatially to the somatotopic representation of the human feet.
Fig. 2
Fig. 2
Time-frequency plots illustrating the amplitude of α (6–10 Hz) oscillations time-locked to S1 and S2 offset for each participant group (TL = infants at typical likelihood of ASD or ADHD; EL-ADHD = infants at elevated likelihood of ADHD; EL-ASD = infants at elevated likelihood of ASD; EL-ASD+ADHD = infants at elevated likelihood of ASD and ADHD). Black dotted rectangles indicate the first and second vibrotactile stimulations. Red dotted squares indicate the 500-ms-long time-windows post-stimulus offset selected for statistical analysis. Amplitude scale is − 0.5, 0.5 μv
Fig. 3
Fig. 3
Boxplots illustrating the amplitude of α (6–10 Hz) oscillations time-locked to S1 and S2 offset for each participant group (green = infants at typical likelihood of ASD or ADHD; violet = infants at elevated likelihood of ASD; grey = infants at elevated likelihood of ADHD; orange = infants at elevated likelihood of ASD and ADHD). A significant reduction in α desynchronization with repeated tactile stimulation occurred only in TL infants. **p < .001
Fig. 4
Fig. 4
Boxplot illustrating the tactile suppression index, α (6–10 Hz), for each participant group (green = infants at typical likelihood of ASD or ADHD; violet = infants at elevated likelihood of ASD; grey = infants at elevated likelihood of ADHD; orange = infants at elevated likelihood of ASD and ADHD). *p < .05
Fig. 5
Fig. 5
Scatterplots illustrating the associations between tactile suppression index (S2–S1 α amplitude) at 10 months and a ADOS-2 CSS at 24 months (p < .001), b ECBQ activity at 24 months (p = ns) and c ECBQ inhibitory control at 24 months (p = ns). Groups are illustrated with different colours (green = infants at typical likelihood of ASD or ADHD; violet = infants at elevated likelihood of ASD; grey = infants at elevated likelihood of ADHD; orange = infants at elevated likelihood of ASD and ADHD). Notes: (1) Fit lines are presented for an average of all infants. (2) The participant with a TSI < − 1 in a does not appear in b and c since this infant did not contribute ECBQ data
Fig. 6
Fig. 6
a Scatterplot illustrating the moderating effect of tactile sensory seeking (10 months) on the association between tactile suppression index (S2–S1 α amplitude) at 10 months and ADOS-2 CSS at 24 months. b Plot of simple slopes illustrating the interaction effect of tactile sensory seeking: the association between tactile suppression index and ADOS-2 CSS (log) is significant for average and low tactile sensory seeking (p < .001) but not significant for high tactile sensory seeking (p = .688). c Johnson-Neyman plot illustrating the region of significance of the moderator: the association between tactile suppression index and ADOS-2 CSS (log) is not significant for values of tactile sensory seeking ≤ 2.13 (i.e. high tactile seeking)
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