Sleep Problems in Preschoolers With Autism Spectrum Disorder Are Associated With Sensory Sensitivities and Thalamocortical Overconnectivity

2013 Grove, 2019, Identification of common genetic risk variants for autism spectrum disorder, Nat Genet, 51, 431, 10.1038/s41588-019-0344-8 Gazestani, 2019, A perturbed gene network containing PI3K–AKT, RAS–ERK and WNT–β-catenin pathways in leukocytes is linked to ASD genetics and symptom severity, Nat Neurosci, 22, 1624, 10.1038/s41593-019-0489-x Courchesne, 2020, Prenatal origins of ASD: The when, what, and how of ASD development, Trends Neurosci, 43, 326, 10.1016/j.tins.2020.03.005 Hull, 2017, Resting-state functional connectivity in autism spectrum disorders: A review, Front Psychiatry, 7, 205, 10.3389/fpsyt.2016.00205 Holiga, 2019, Patients with autism spectrum disorders display reproducible functional connectivity alterations, Sci Transl Med, 11, 10.1126/scitranslmed.aat9223 Müller, 2014, Anatomical and functional connectivity in autism spectrum disorders, 49 Kanold, 2010, The subplate and early cortical circuits, Annu Rev Neurosci, 33, 23, 10.1146/annurev-neuro-060909-153244 Kostović, 2010, The development of the subplate and thalamocortical connections in the human foetal brain, Acta Paediatr, 99, 1119, 10.1111/j.1651-2227.2010.01811.x Kostović, 2011, Developmental history of the subplate zone, subplate neurons and interstitial white matter neurons: Relevance for schizophrenia, Int J Dev Neurosci, 29, 193, 10.1016/j.ijdevneu.2010.09.005 O’Leary, 2002, Patterning centers, regulatory genes and extrinsic mechanisms controlling arealization of the neocortex, Curr Opin Neurobiol, 12, 14, 10.1016/S0959-4388(02)00285-4 Constantinople, 2013, Deep cortical layers are activated directly by thalamus, Science, 340, 1591, 10.1126/science.1236425 Hoerder-Suabedissen, 2015, Development, evolution and pathology of neocortical subplate neurons, Nat Rev Neurosci, 16, 133, 10.1038/nrn3915 Luhmann, 2018, The superior function of the subplate in early neocortical development, Front Neuroanat, 12, 97, 10.3389/fnana.2018.00097 Hadders-Algra, 2018, Early human brain development: Starring the subplate, Neurosci Biobehav Rev, 92, 276, 10.1016/j.neubiorev.2018.06.017 Kanold, 2019, The first cortical circuits: Subplate neurons lead the way and shape cortical organization, Neuroforum, 25, 15, 10.1515/nf-2018-0010 Bai, 2019, Association of genetic and environmental factors with autism in a 5-country cohort, JAMA Psychiatry, 76, 1035, 10.1001/jamapsychiatry.2019.1411 Sandin, 2017, The heritability of autism spectrum disorder, JAMA, 318, 1182, 10.1001/jama.2017.12141 Colvert, 2015, Heritability of autism spectrum disorder in a UK population-based twin sample, JAMA Psychiatry, 72, 415, 10.1001/jamapsychiatry.2014.3028 Lombardo, 2018, Maternal immune activation dysregulation of the fetal brain transcriptome and relevance to the pathophysiology of autism spectrum disorder, Mol Psychiatry, 23, 1001, 10.1038/mp.2017.15 Al-Haddad, 2019, Long-term risk of neuropsychiatric disease after exposure to infection in utero, JAMA Psychiatry, 76, 594, 10.1001/jamapsychiatry.2019.0029 Agrawal, 2018, Prevalence of autism spectrum disorder in preterm infants: A meta-analysis, Pediatrics, 142, 10.1542/peds.2018-0134 Chien, 2019, Prenatal and perinatal risk factors and the clinical implications on autism spectrum disorder, Autism, 23, 783, 10.1177/1362361318772813 Getahun, 2017, Association of perinatal risk factors with autism spectrum disorder, Am J Perinatol, 34, 295, 10.1055/s-0036-1597624 Hoerder-Suabedissen, 2013, Expression profiling of mouse subplate reveals a dynamic gene network and disease association with autism and schizophrenia, Proc Natl Acad Sci U S A, 110, 3555, 10.1073/pnas.1218510110 Toulmin, 2015, Specialization and integration of functional thalamocortical connectivity in the human infant, Proc Natl Acad Sci U S A, 112, 6485, 10.1073/pnas.1422638112 Mikhailova, 2017, Unbiased quantification of subplate neuron loss following neonatal hypoxia-ischemia in a rat model, Dev Neurosci, 39, 171, 10.1159/000460815 Kanold, 2003, Role of subplate neurons in functional maturation of visual cortical columns, Science, 301, 521, 10.1126/science.1084152 McQuillen, 2003, Selective vulnerability of subplate neurons after early neonatal hypoxia-ischemia, J Neurosci, 23, 3308, 10.1523/JNEUROSCI.23-08-03308.2003 Materna, 2008, Dissociable roles of the superior temporal sulcus and the intraparietal sulcus in joint attention: A functional magnetic resonance imaging study, J Cogn Neurosci, 20, 108, 10.1162/jocn.2008.20008 McClendon, 2017, Transient hypoxemia chronically disrupts maturation of preterm fetal ovine subplate neuron arborization and activity, J Neurosci, 37, 11912, 10.1523/JNEUROSCI.2396-17.2017 Caubit, 2016, TSHZ3 deletion causes an autism syndrome and defects in cortical projection neurons, Nat Genet, 48, 1359, 10.1038/ng.3681 Hutsler, 2015, The relevance of subplate modifications to connectivity in the cerebral cortex of individuals with autism spectrum disorders, 201 Hutsler, 2016, Review: Cortical construction in autism spectrum disorder: Columns, connectivity and the subplate, Neuropathol Appl Neurobiol, 42, 115, 10.1111/nan.12227 Kanold, 2009, Subplate neurons: Crucial regulators of cortical development and plasticity, Front Neuroanat, 3, 16, 10.3389/neuro.05.016.2009 Nagode, 2017, Abnormal development of the earliest cortical circuits in a mouse model of autism spectrum disorder, Cell Rep, 18, 1100, 10.1016/j.celrep.2017.01.006 Wess, 2017, Subplate neurons are the first cortical neurons to respond to sensory stimuli, Proc Natl Acad Sci U S A, 114, 12602, 10.1073/pnas.1710793114 Serati, 2019, The role of the subplate in schizophrenia and autism: A systematic review, Neuroscience, 408, 58, 10.1016/j.neuroscience.2019.03.049 Stoner, 2014, Patches of disorganization in the neocortex of children with autism, N Engl J Med, 370, 1209, 10.1056/NEJMoa1307491 McFadden, 2013, Evidence for dysregulation of axonal growth and guidance in the etiology of ASD, Front Hum Neurosci, 7, 671, 10.3389/fnhum.2013.00671 Anomal, 2015, Impaired processing in the primary auditory cortex of an animal model of autism, Front Syst Neurosci, 9, 158, 10.3389/fnsys.2015.00158 Alcauter, 2014, Development of thalamocortical connectivity during infancy and its cognitive correlations, J Neurosci, 34, 9067, 10.1523/JNEUROSCI.0796-14.2014 Ferradal, 2019, System-specific patterns of thalamocortical connectivity in early brain development as revealed by structural and functional MRI, Cereb Cortex, 29, 1218, 10.1093/cercor/bhy028 Doria, 2010, Emergence of resting state networks in the preterm human brain, Proc Natl Acad Sci U S A, 107, 20015, 10.1073/pnas.1007921107 Jakab, 2014, Fetal functional imaging portrays heterogeneous development of emerging human brain networks, Front Hum Neurosci, 8, 852, 10.3389/fnhum.2014.00852 Thomason, 2013, Cross-hemispheric functional connectivity in the human fetal brain, Sci Transl Med, 5, 173ra24, 10.1126/scitranslmed.3004978 Barkat, 2011, A critical period for auditory thalamocortical connectivity, Nat Neurosci, 14, 1189, 10.1038/nn.2882 Thomason, 2017, Weak functional connectivity in the human fetal brain prior to preterm birth, Sci Rep, 7, 39286, 10.1038/srep39286 Rotem-Kohavi, 2019, Alterations in resting-state networks following in utero selective serotonin reuptake inhibitor exposure in the neonatal brain, Biol Psychiatry Cogn Neurosci Neuroimaging, 4, 39 Ferri, 2003, The mismatch negativity and the P3a components of the auditory event-related potentials in autistic low-functioning subjects, Clin Neurophysiol, 114, 1671, 10.1016/S1388-2457(03)00153-6 Hudac, 2018, Early enhanced processing and delayed habituation to deviance sounds in autism spectrum disorder, Brain Cogn, 123, 110, 10.1016/j.bandc.2018.03.004 Schwartz, 2018, Meta-analysis and systematic review of the literature characterizing auditory mismatch negativity in individuals with autism, Neurosci Biobehav Rev, 87, 106, 10.1016/j.neubiorev.2018.01.008 Yoshimura, 2016, Synchrony of auditory brain responses predicts behavioral ability to keep still in children with autism spectrum disorder: Auditory-evoked response in children with autism spectrum disorder, Neuroimage Clin, 12, 300, 10.1016/j.nicl.2016.07.009 Gomot, 2006, Change detection in children with autism: An auditory event-related fMRI study, Neuroimage, 29, 475, 10.1016/j.neuroimage.2005.07.027 Green, 2015, Neurobiology of sensory overresponsivity in youth with autism spectrum disorders, JAMA Psychiatry, 72, 778, 10.1001/jamapsychiatry.2015.0737 Green, 2017, Reduced modulation of thalamocortical connectivity during exposure to sensory stimuli in ASD, Autism Res, 10, 801, 10.1002/aur.1726 Green, 2019, Distinct patterns of neural habituation and generalization in children and adolescents with autism with low and high sensory overresponsivity, Am J Psychiatry, 176, 1010, 10.1176/appi.ajp.2019.18121333 Tharpe, 2006, Auditory characteristics of children with autism, Ear Hear, 27, 430, 10.1097/01.aud.0000224981.60575.d8 Cerliani, 2015, Increased functional connectivity between subcortical and cortical resting-state networks in autism spectrum disorder, JAMA Psychiatry, 72, 767, 10.1001/jamapsychiatry.2015.0101 Linke, 2018, Children with ASD show links between aberrant sound processing, social symptoms, and atypical auditory interhemispheric and thalamocortical functional connectivity, Dev Cogn Neurosci, 29, 117, 10.1016/j.dcn.2017.01.007 Iidaka, 2019, Thalamocortical hyperconnectivity and amygdala-cortical hypoconnectivity in male patients with autism spectrum disorder, Front Psychiatry, 10, 252, 10.3389/fpsyt.2019.00252 Maximo, 2019, Aberrant “deep connectivity” in autism: A cortico-subcortical functional connectivity magnetic resonance imaging study, Autism Res, 12, 384, 10.1002/aur.2058 Mizuno, 2006, Partially enhanced thalamocortical functional connectivity in autism, Brain Res, 1104, 160, 10.1016/j.brainres.2006.05.064 Nair, 2013, Impaired thalamocortical connectivity in autism spectrum disorder: A study of functional and anatomical connectivity, Brain, 136, 1942, 10.1093/brain/awt079 Nair, 2015, Regional specificity of aberrant thalamocortical connectivity in autism, Hum Brain Mapp, 36, 4497, 10.1002/hbm.22938 Woodward, 2017, Thalamocortical dysconnectivity in autism spectrum disorder: An analysis of the Autism Brain Imaging Data Exchange, Biol Psychiatry Cogn Neurosci Neuroimaging, 2, 76 Anderson, 2005, Thalamic Cav3.1 T-type Ca2+ channel plays a crucial role in stabilizing sleep, Proc Natl Acad Sci U S A, 102, 1743, 10.1073/pnas.0409644102 Cueni, 2008, T-type Ca2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites, Nat Neurosci, 11, 683, 10.1038/nn.2124 Jan, 2009, The role of the thalamus in sleep, pineal melatonin production, and circadian rhythm sleep disorders, J Pineal Res, 46, 1, 10.1111/j.1600-079X.2008.00628.x Steriade, 1993, Thalamocortical oscillations in the sleeping and aroused brain, Science, 262, 679, 10.1126/science.8235588 Picchioni, 2014, Decreased connectivity between the thalamus and the neocortex during human nonrapid eye movement sleep, Sleep, 37, 387, 10.5665/sleep.3422 Spoormaker, 2010, Development of a large-scale functional brain network during human non-rapid eye movement sleep, J Neurosci, 30, 11379, 10.1523/JNEUROSCI.2015-10.2010 Hale, 2016, Altered thalamocortical and intra-thalamic functional connectivity during light sleep compared with wake, Neuroimage, 125, 657, 10.1016/j.neuroimage.2015.10.041 Tagliazucchi, 2012, Automatic sleep staging using fMRI functional connectivity data, Neuroimage, 63, 63, 10.1016/j.neuroimage.2012.06.036 Tagliazucchi, 2014, Decoding wakefulness levels from typical fMRI resting-state data reveals reliable drifts between wakefulness and sleep, Neuron, 82, 695, 10.1016/j.neuron.2014.03.020 Mitra, 2015, Propagated infra-slow intrinsic brain activity reorganizes across wake and slow wave sleep, Elife, 4, 10.7554/eLife.10781 Mitra, 2017, Resting-state fMRI in sleeping infants more closely resembles adult sleep than adult wakefulness, PLoS One, 12, 10.1371/journal.pone.0188122 Arazi, 2020, Reduced sleep pressure in young children with autism, Sleep, 43, zsz309, 10.1093/sleep/zsz309 Carmassi, 2019, Systematic review of sleep disturbances and circadian sleep desynchronization in autism spectrum disorder: Toward an integrative model of a self-reinforcing loop, Front Psychiatry, 10, 366, 10.3389/fpsyt.2019.00366 Reynolds, 2019, Sleep problems in 2- to 5-year-olds with autism spectrum disorder and other developmental delays, Pediatrics, 143, 10.1542/peds.2018-0492 Sivertsen, 2012, Sleep problems in children with autism spectrum problems: A longitudinal population-based study, Autism, 16, 139, 10.1177/1362361311404255 Richdale, 2009, Sleep problems in autism spectrum disorders: Prevalence, nature, & possible biopsychosocial aetiologies, Sleep Med Rev, 13, 403, 10.1016/j.smrv.2009.02.003 Mannion, 2014, Sleep problems in autism spectrum disorder: A literature review, Rev J Autism Dev Disord, 1, 101, 10.1007/s40489-013-0009-y Krakowiak, 2008, Sleep problems in children with autism spectrum disorders, developmental delays, and typical development: A population-based study, J Sleep Res, 17, 197, 10.1111/j.1365-2869.2008.00650.x Sikora, 2012, The relationship between sleep problems and daytime behavior in children of different ages with autism spectrum disorders, Pediatrics, 130, S83, 10.1542/peds.2012-0900F Mazzone, 2018, The relationship between sleep problems, neurobiological alterations, core symptoms of autism spectrum disorder, and psychiatric comorbidities, J Clin Med, 7, 102 Tzischinsky, 2018, Sleep disturbances are associated with specific sensory sensitivities in children with autism, Mol Autism, 9, 22, 10.1186/s13229-018-0206-8 Zou, 2008, An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: Fractional ALFF, J Neurosci Methods, 172, 137, 10.1016/j.jneumeth.2008.04.012 Zuo, 2010, The oscillating brain: Complex and reliable, Neuroimage, 49, 1432, 10.1016/j.neuroimage.2009.09.037 Del Felice, 2012, The gating role of the thalamus to protect sleep: An f-MRI report, Sleep Med, 13, 447, 10.1016/j.sleep.2011.07.021 Freedman, 2020, P50 inhibitory sensory gating in schizophrenia: Analysis of recent studies, Schizophr Res, 218, 93, 10.1016/j.schres.2020.02.003 Ozonoff, 2015, Diagnostic stability in young children at risk for autism spectrum disorder: A baby siblings research consortium study, J Child Psychol Psychiatry, 56, 988, 10.1111/jcpp.12421 Lord, 2012 Rutter, 2003 Achenbach, 2000 Gregory, 2011, Sleep items in the child behavior checklist: A comparison with sleep diaries, actigraphy, and polysomnography, J Am Acad Child Adolesc Psychiatry, 50, 499, 10.1016/j.jaac.2011.02.003 Dunn, 2014 White, 2010, PROMO: Real-time prospective motion correction in MRI using image-based tracking, Magn Reson Med, 63, 91, 10.1002/mrm.22176 Kumar, 2017, Functional anatomy of the human thalamus at rest, Neuroimage, 147, 678, 10.1016/j.neuroimage.2016.12.071 Hwang, 2017, The human thalamus is an integrative hub for functional brain networks, J Neurosci, 37, 5594, 10.1523/JNEUROSCI.0067-17.2017 Cortesi, 2010, Sleep in children with autistic spectrum disorder, Sleep Med, 11, 659, 10.1016/j.sleep.2010.01.010 Reynolds, 2011, Sleep and autism spectrum disorders, Pediatr Clin North Am, 58, 685, 10.1016/j.pcl.2011.03.009 Schulz, 2020, Differentiating between sensory sensitivity and sensory reactivity in relation to restricted interests and repetitive behaviours, Autism, 24, 121, 10.1177/1362361319850402 Dunn, 1999 Schoen, 2008, Pilot study of the sensory over-responsivity scales: Assessment and inventory, Am J Occup Ther, 62, 393, 10.5014/ajot.62.4.393 Constantin, 2020, Altered brain-wide auditory networks in a zebrafish model of fragile X syndrome, BMC Biol, 18, 125, 10.1186/s12915-020-00857-6 Kanold, 2019, The integrative function of silent synapses on subplate neurons in cortical development and dysfunction, Front Neuroanat, 13, 41, 10.3389/fnana.2019.00041 Molnár, 2020, Transient cortical circuits match spontaneous and sensory-driven activity during development, Science, 370, 10.1126/science.abb2153 Nair, 2021, Altered thalamocortical connectivity in 6-week-old infants at high familial risk for autism spectrum disorder, Cereb Cortex, 31, 4191, 10.1093/cercor/bhab078 Wolff, 2017, Neural circuitry at age 6 months associated with later repetitive behavior and sensory responsiveness in autism, Mol Autism, 8, 8, 10.1186/s13229-017-0126-z Kolesnik, 2019, Increased cortical reactivity to repeated tones at 8 months in infants with later ASD, Transl Psychiatry, 9, 46, 10.1038/s41398-019-0393-x Humphreys, 2014, Sleep patterns in children with autistic spectrum disorders: A prospective cohort study, Arch Dis Child, 99, 114, 10.1136/archdischild-2013-304083 Nguyen, 2018, Prospective associations between infant sleep at 12 months and autism spectrum disorder screening scores at 24 months in a community-based birth cohort, J Clin Psychiatry, 79, 16m11127, 10.4088/JCP.16m11127 MacDuffie, 2020, Sleep onset problems and subcortical development in infants later diagnosed with autism spectrum disorder, Am J Psychiatry, 177, 518, 10.1176/appi.ajp.2019.19060666 Woodward, 2012, Thalamocortical dysconnectivity in schizophrenia, Am J Psychiatry, 169, 1092, 10.1176/appi.ajp.2012.12010056 Skåtun, 2018, Thalamo-cortical functional connectivity in schizophrenia and bipolar disorder, Brain Imaging Behav, 12, 640, 10.1007/s11682-017-9714-y Chen, 2019, Association between thalamocortical functional connectivity abnormalities and cognitive deficits in schizophrenia, Sci Rep, 9, 2952, 10.1038/s41598-019-39367-z Baran, 2019, Increased thalamocortical connectivity in schizophrenia correlates with sleep spindle deficits: Evidence for a common pathophysiology, Biol Psychiatry Cogn Neurosci Neuroimaging, 4, 706 Farmer, 2018, Spindle activity in young children with autism, developmental delay, or typical development, Neurology, 91, e112, 10.1212/WNL.0000000000005759