Auerbach, Benjamin D

Contractor, Anis

Ethell, Iryna M

Ethridge, Lauren E

McCullagh, Elizabeth A

Pedapati, Ernest V

English

eScholarship - University of California

UC RiversideUC Riverside Previously Published WorksTitleEditorial: Neural markers of sensory processing in developmentPermalinkhttps://escholarship.org/uc/item/2b07n7r8AuthorsEthridge, Lauren EAuerbach, Benjamin DContractor, Aniset al.Publication Date2023DOI10.3389/fnint.2023.1256437 Peer reviewedeScholarship.org Powered by the California Digital LibraryUniversity of CaliforniaTYPE EditorialPUBLISHED 21 July 2023DOI 10.3389/fnint.2023.1256437OPEN ACCESSEDITED AND REVIEWED BYElizabeth B. Torres,Rutgers, The State University of New Jersey,United States*CORRESPONDENCELauren E. Ethridgelauren-ethridge@ouhsc.eduRECEIVED 10 July 2023ACCEPTED 12 July 2023PUBLISHED 21 July 2023CITATIONEthridge LE, Auerbach BD, Contractor A,Ethell IM, McCullagh EA and Pedapati EV (2023)Editorial: Neural markers of sensory processingin development.Front. Integr. Neurosci. 17:1256437.doi: 10.3389/fnint.2023.1256437COPYRIGHT© 2023 Ethridge, Auerbach, Contractor, Ethell,McCullagh and Pedapati. This is anopen-access article distributed under the termsof the Creative Commons Attribution License(CC BY). The use, distribution or reproductionin other forums is permitted, provided theoriginal author(s) and the copyright owner(s)are credited and that the original publication inthis journal is cited, in accordance withaccepted academic practice. No use,distribution or reproduction is permitted whichdoes not comply with these terms.Editorial: Neural markers ofsensory processing indevelopmentLauren E. Ethridge1,2*, Benjamin D. Auerbach3, Anis Contractor4,Iryna M. Ethell5, Elizabeth A. McCullagh6 and Ernest V. Pedapati7,81Department of Psychology, University of Oklahoma, Norman, OK, United States, 2Department ofPediatrics, University of Oklahoma Health Sciences Center, Oklahoma City, OK, United States,3Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign,Champaign, IL, United States, 4Department of Neuroscience, Psychiatry and Behavioral Sciences, andNeurobiology, Northwestern University, Evanston, IL, United States, 5Department of BiomedicalSciences, University of California, Riverside, Riverside, CA, United States, 6Department of IntegrativeBiology, Oklahoma State University, Stillwater, OK, United States, 7Department of Psychiatry andBehavioral Neuroscience, College of Medicine, University of Cincinnati, Cincinnati, OH, United States,8Division of Child and Adolescent Psychiatry, and Child Neurology, Cincinnati Children’s HospitalMedical Center, Cincinnati, OH, United StatesKEYWORDSneurodevelopment, translational methods, EEG, neurodevelopmental disorders, sensorysystemsEditorial on the Research TopicNeural markers of sensory processing in developmentIntroductionSensory processing dynamics have emerged as important contributors to typicalcognitive and social development (Larkin et al., 2017; Cruz et al., 2022). In addition, sensoryprocessing abnormalities are common in neurodevelopmental disorders, particularly inautism spectrum disorders (ASDs; Robertson and Baron-Cohen, 2017) and related geneticdisorders like Fragile X Syndrome (FXS; Rais et al., 2018). This Research Topic exploresthe determinants of early sensory system maturation, functional consequences of changesto sensory development, and methodologies to investigate under-studied modalities ofsensation to further the understanding of the role of sensory systems in a range offunctional outcomes.Electroencephalography (EEG) in sensory systemsresearchEEG is a frequently employed method in the translational neuroscience of sensorysystems. EEG provides a direct measure of neural oscillatory patterns on a millisecondtime-scale consistent with the speed at which sensory systems operate to detect and processinformation. EEG is safe and well-tolerated, and data can be readily collected from infantand clinical populations while awake and performing a task. Local field potentials, suchas measured in aggregate with EEG, are easily bridged to animal models for circuit-levelFrontiers in IntegrativeNeuroscience 01 frontiersin.orgEthridge et al. 10.3389/fnint.2023.1256437investigation of neural findings conserved across species. An et al.found that children demonstrated minimal habituation to repeatedtones; however, improved language ability in children with FXSwas associated with increased habituation in the frontal cortex. Thehabituation task, which shows conservation across species in FXS(Lovelace et al., 2016) is thought to represent a proxy of auditoryhypersensitivity (Ethridge et al., 2016), and the findings suggest thatthis aspect of auditory systemmaturation is more critical in atypicalthan typical development for language acquisition.Sensory processing changes in NDDsSubtle sensory processing changes may mediate atypicaldevelopmental trajectories even in neurodevelopmental disorderswhere sensory symptoms are not at the forefront, or may beindicative of neural changes related to early developmentalevents. Witteveen et al. examined the 1/f aperiodic slope ofEEG spectrograms in healthy infants as a proxy for maturationand found advanced maturation was consistent with birth,rather than gestational age, triggering changes in visual cortexactivity. These effects were recapitulated in local field potentialrecordings of preterm mice, driven by enhanced inhibitionvia changes to distribution of parvalbumin expression levelsin PV-expressing interneurons. This conservation of visualcortical activity with preterm birth suggests that maturationof the power spectrum in primary visual cortex may be animportant indicator of sensory system development relevant tofuture assessment of neurocognitive outcomes. It is, however,unclear at this point whether these changes to visual systemmaturation are driven by environmental changes (birth)alone, or by other factors contributing to increased chance ofpreterm birth.Much work has been done in this area describing typicaldevelopment in humans and animal models for visual and auditorymodalities, however, gaps remain in understanding how thesemeasures correspond across species over various developmentalperiods. Significant gaps also persist in describing the developmentof thesemeasures in sensorymodalities beyond vision and audition.In particular, the ability to deliver visual and auditory stimuliwith high precision may partially account for the preponderanceof neuroimaging and EEG developmental studies in the visualand auditory domains, rather than enhanced importance of thesedomains to developmental outcomes (Espenhahn et al., 2021;Ahlfors et al., 2022; Arpaia et al., 2022). Bhattacharjee et al.describe the development of a novel tactile stimulus deliverysystem to enable measurement of active somatosensation with theprecision necessary to enable use in EEG,magnetoencephalography(MEG), and other neurophysiology studies. Tactile hypersensitivityis commonly reported in ASDs, but the neural correlates anddevelopment of the tactile system is severely understudied in ASD(Marco et al., 2011). Technological enhancements like the onesreported here will enable researchers to provide a more balancedinvestigation of sensory systems and their neural correlates acrossboth typical and atypical development.Finally, it is important to note that studying the neuralcorrelates of sensory systems is critically hampered by thelack of psychometrically sound measures for characterizingsensory behaviors in both humans and animal models. Thisis a strong limitation to what degree we can map clinicalalterations in sensation to brain activity. Mulligan et al.,describe overlapping phenotypes in children with idiopathicsensory processing disorder, with the majority of childrenshowing a combination of multiple sub-types, suggesting thatcurrent methodology for classifying sensory behaviors in humansrequires further study to develop categories useful for assessingdevelopmental trajectories and outcomes and for mapping toneural measures.In summary, understanding sensory system development is ofcritical importance for predicting functional outcomes across avariety of linked constructs in both neurodevelopmental disordersand typical development. Translational work using methodologiessuch as EEG can provide significant insight into neural correlatesof sensory processing, and is feasible in both developmentalhuman populations and animal models, allowing further studyinto circuit and molecular mechanisms for sensory systemmodulation. However, study in this area is limited by technologicaladvancements in some sensory modalities more than others, anda lack of strong assessment methodology for quantifying sensorybehaviors. Advancement in these areas is critically needed toincorporate already translationally sophisticated neuroimaging andneurophysiological methods into a comprehensive view of sensorysystem development.Author contributionsAll authors listed have made a substantial, direct, andintellectual contribution to the work and approved itfor publication.Conflict of interestThe authors declare that the research was conducted in theabsence of any commercial or financial relationships that could beconstrued as a potential conflict of interest.Publisher’s noteAll claims expressed in this article are solely those of theauthors and do not necessarily represent those of their affiliatedorganizations, or those of the publisher, the editors and thereviewers. Any product that may be evaluated in this article, orclaim that may be made by its manufacturer, is not guaranteed orendorsed by the publisher.Frontiers in IntegrativeNeuroscience 02 frontiersin.orgEthridge et al. 10.3389/fnint.2023.1256437ReferencesAhlfors, S. P., Graham, S., Alho, J., Joseph, R. M., McGuiggan, N. M., Nayal, Z.,et al. (2022). Magnetoencephalography and electroencephalography can both detectdifferences in cortical responses to vibrotactile stimuli in individuals on the autismspectrum. Front. Psychiatry 13, 902332. doi: 10.3389/fpsyt.2022.902332Arpaia, P., Cataldo, A., Criscuolo, S., De Benedetto, E., Masciullo, A., Schiavoni, R.,et al. (2022). Assessment and scientific progresses in the analysis of olfactory evokedpotentials. Bioengineering 9, 252. doi: 10.3390/bioengineering9060252Cruz, S., Lifter, K., Barros, C., Vieira, R., and Sampaio, A. (2022). Neuraland psychophysiological correlates of social communication development:evidence from sensory processing, motor, cognitive, language and emotionalbehavioral milestones across infancy. Appl. Neuropsychol. Child 11, 158–177.doi: 10.1080/21622965.2020.1768392Espenhahn, S., Godfrey, K. J., Kaur, S., Ross, M., Nath, N., Dmitrieva,O., et al. (2021). Tactile cortical responses and association with tactilereactivity in young children on the autism spectrum. Mol. Autism. 12, 26.doi: 10.1186/s13229-021-00435-9Ethridge, L. E., White, S. P., Mosconi, M. W., Wang, J., Byerly, M. J., Sweeney, J.A., et al. (2016). Reduced habituation of auditory evoked potentials indicate corticalhyper-excitability in Fragile X Syndrome. Transl. Psychiatry 6, e787. doi: 10.1038/tp.2016.48Larkin, F., Meins, E., Centifanti, L. C. M., Fernyhough, C., and Leekam, S. R. (2017).How does restricted and repetitive behavior relate to language and cognition in typicaldevelopment? Dev. Psychopathol. 29, 863–874. doi: 10.1017/S0954579416000535Lovelace, J. W., Wen, T. H., Reinhard, S., Hsu, M. S., Sidhu, H., Ethell, I. M.,et al. (2016). Matrix metalloproteinase-9 deletion rescues auditory evoked potentialhabituation deficit in a mouse model of Fragile X Syndrome. Neurobiol. Dis. 89,126–135. doi: 10.1016/j.nbd.2016.02.002Marco, E. J., Hinkley, L. B., Hill, S. S., and Nagarajan, S. S. (2011). Sensoryprocessing in autism: a review of neurophysiologic findings. Pediatr. Res. 69, 48R−54R.doi: 10.1203/PDR.0b013e3182130c54Rais, M., Binder, D. K., Razak, K. A., and Ethell, I. M. (2018). Sensoryprocessing phenotypes in fragile X syndrome. ASN Neuro. 10, 1759091418801092.doi: 10.1177/1759091418801092Robertson, C. E., and Baron-Cohen, S. (2017). Sensory perception in autism. Nat.Rev. Neurosci. 18, 671–684. doi: 10.1038/nrn.2017.112Frontiers in IntegrativeNeuroscience 03 frontiersin.org© 2023. This work is licensed underhttp://creativecommons.org/licenses/by/4.0/ (the “License”).  Notwithstandingthe ProQuest Terms and Conditions, you may use this content in accordancewith the terms of the License.

Editorial: Neural markers of sensory processing in development

Abstract

Similar works

Full text

Available Versions

eScholarship - University of California

Crossref