Study at a glance
- Authors: Rebecca F. Schwarzlose, Rebecca Tillman, Caroline P. Hoyniak, Joan L. Luby, Deanna M. Barch
- Year: 2023
- Journal: Biological Psychiatry
- DOI: 10.1016/j.biopsych.2022.09.004
- N: 11,210 children (ABCD Study, ages 9–12); FC subsets 7,760 (Y0 exploratory) / 5,117 (Y2 preregistered)
- Design: Longitudinal community cohort (ABCD); linear mixed-effects models; resting-state fMRI functional connectivity with preregistered two-timepoint replication (OSF)
Key findings
- Sensory over-responsivity (SOR) — atypical negative reactions to innocuous exteroceptive stimuli (sounds, textures, smells) — affected 18% of the sample (12% mild, 6% severe) yet comprised 57% of children with clinically-range internalizing or externalizing symptoms (65% of internalizing, 52% of externalizing).
- Controlling for autistic traits (SCI + RRB), both mild and severe SOR were associated with greater concurrent depression, anxiety, OCD and ADHD symptoms in a stepwise none<mild<severe pattern; SOR was negatively associated with conduct-disorder symptoms — a differential (not blanket) association that argues against a pure emotion-dysregulation account.
- Longitudinally, SOR predicted increased anxiety (mild & severe), ADHD (mild) and prodromal-psychosis (severe) symptoms one year later, controlling for concurrent symptoms and autistic traits — the sensory-specific account’s key prediction: SOR carries unique predictive information beyond both psychiatric symptoms and autistic traits.
- 15 resting-state functional-connectivity differences were reliably associated with severe SOR across scans collected 2 years apart, surviving covariates for sex, age, economic disadvantage, autistic traits and psychiatric symptoms: reduced FC within/between sensorimotor networks; enhanced sensorimotor-hand↔**salience** FC and within–ventral-attention FC; enhanced cingulo-opercular↔**Amygdala** FC; and altered sensory-network↔hippocampus FC.
- Reads the FC profile through a sensory-prediction lens (converging with Sinha et al.’s ‘autism as a disorder of prediction’): hippocampal–sensory-cortex coupling supports prediction and experience-based modulation of sensory processing, so atypical hippocampal-sensory FC may impair adaptive modulation of sensory input — a predictive account of an exteroceptive over-responsivity.
Limitations
- SOR measured by a single parent-report Likert item (‘Seems overly sensitive to sounds, textures, or smells’) from the Short-SRS, never validated against multi-item SOR instruments (e.g. Sensory Processing 3-Dimensions); autistic traits likewise from an abbreviated scale.
- FC analyses restricted to no-vs-severe SOR to maximize group differences; the conservative two-timepoint replication improves reliability but prevents modeling FC change over time.
- ABCD was not designed to recruit children with SOR; those with auditory SOR may be underrepresented (scanner-noise dropout), which the authors flag as a reason the sensorimotor-hand (tactile) network dominated.
- Correlational FC with no cognitive inference from activation; excludes children with ASD requiring special schooling, so generality to that group is untested.
- SOR is an exteroceptive phenomenon — its relevance to this interoception wiki is as a parallel/boundary case, not a direct interoceptive result (see Exteroception Boundary).
Connections
- Methods: Resting-state functional connectivity
- Concepts: Sensory over-responsivity (SOR), Salience network, Exteroception Boundary, Interoceptive psychopathology, Amygdala, Predictive coding, Multisensory integration, Cortical somatotopy (the homunculus)
- Debates: Is interoception domain-general or organ-specific?
- Related studies: Nord et al. (2021), Barr et al. (2022), Quadt et al. (2018)
Not an interoception study. SOR is over-responsivity to exteroceptive stimuli — sounds, textures, smells — so this paper is filed the way the wiki files Zeharia et al. (2019) and Barr et al. (2022): as a boundary/parallel case, useful precisely because it runs the interoception literature’s own transdiagnostic-marker logic in the exteroceptive domain, in a sample (N=11,210, ABCD) an order of magnitude larger than any interoceptive study here. Read it against Nord, Lawson & Dalgleish (2021) — the interoceptive counterpart — and the two together frame the question this wiki keeps circling: is there a sensory (as opposed to affective or cognitive) transdiagnostic pathway into psychopathology, and does it run through the same salience machinery on both sides of the skin?
What it did
Parent-reported SOR (one Short-SRS item) was used to sort 11,210 ABCD children into no (82%), mild (12%) and severe (6%) SOR groups. Linear mixed-effects models (family nested within site) then tested SOR group against demographics, autistic traits (social-communication impairment SCI, restricted/repetitive behaviour RRB), and dimensional psychiatric symptoms (CBCL depression, anxiety, OCD, ADHD, ODD, CD; PQ-BC prodromal psychosis), both concurrently (Y1) and one year later (Y2). The design’s discipline is an incremental covariate approach: significant SOR–symptom effects were re-tested with SCI added, then RRB added, with FDR correction at each step — so a surviving effect is one that is not reducible to subthreshold autistic traits.
The neural arm used resting-state fMRI: exploratory FC screening in the Y0 dataset (7,760 children) identified 21 network-pair candidates, preregistered (OSF) for independent replication in the Y2 dataset (5,117 children); 17 replicated, 15 survived stringent post-hoc covariates. Cortex was parcellated with the Gordon scheme into 13 functional networks; connectivity was network-averaged BOLD correlation.
The three-accounts framing
The paper is built around adjudicating three explanations of why SOR co-occurs with psychopathology — a cleaner version of the cause-or-consequence problem that Interoceptive psychopathology keeps hitting:
| account | claim | prediction |
|---|---|---|
| dysregulation | SOR is a behavioural readout of transdiagnostic emotion dysregulation | SOR adds no information beyond existing symptoms; associations are uniform across disorders |
| autism | SOR–symptom links are driven by subthreshold autistic traits | SOR adds nothing beyond autistic traits |
| sensory-specific | SOR is a neurobiological sensory-processing difference and an independent risk factor | SOR predicts symptoms beyond both symptoms and autistic traits, and has a sensory neural signature |
The data land on the sensory-specific account: associations are differential not uniform (positive for anxiety/depression/OCD/ADHD, negative for conduct disorder), survive autistic-trait control, predict future anxiety prospectively, and carry a sensory-network FC signature. The dysregulation and autism accounts are both rejected as sufficient.
Where it lands in the wiki
On Sensory over-responsivity (SOR) (created here) — the construct’s home page, holding the prevalence, the three accounts, and the FC profile.
On Exteroception Boundary. SOR is the exteroceptive mirror of the interoceptive over-responsivity the wiki carries (panic’s cardiac hypervigilance, anxiety sensitivity). That the same nodes — salience, ventral attention, Amygdala — show altered connectivity for exteroceptive over-responsivity as the interoceptive literature implicates for internal over-attention is the kind of cross-boundary convergence that the boundary page argues should make us cautious about treating “interoceptive” and “exteroceptive” salience as separate systems.
On Salience network. The salience network here does its Barrett/Menon job in a developmental clinical population: enhanced sensorimotor↔salience coupling is read as the network assigning behavioural relevance to innocuous sensory input that should have been ignored — over-precision on exteroceptive prediction error, the exteroceptive analogue of the interoceptive precision failures on computational psychosomatics.
On Interoceptive psychopathology and Nord et al. (2021). A transdiagnostic sensory marker with a prospective-risk claim and a candidate neural signature — exactly the shape of the interoceptive mid-insula story, in the exteroceptive domain and with a far larger sample. The parallel is instructive and a caution: if an exteroceptive sensory feature predicts the same broad psychopathology transdiagnostically, then “interoceptive dysfunction across disorders” may be one instance of a more general sensory-precision dysfunction, not an interoception-specific mechanism.
Brakes
The whole edifice rests on a single parent-report item, never validated against real SOR instruments — the authors concede this first among limitations. The FC findings are correlational, the sensorimotor-hand emphasis may be an artefact of the item’s wording (or of auditory-SOR dropout under scanner noise), and the design cannot separate cause from consequence any better than the interoceptive literature it parallels — a prospective association is not a causal one. And it is, throughout, about the outside of the body: its value to this wiki is comparative, not confirmatory.