The serotonin system in autism spectrum disorder: From biomarker to animal models

Muller, C.L.; Anacker, A.M.J.; Veenstra-VanderWeele, J.

doi:10.1016/j.neuroscience.2015.11.010

Cited by 531Autism Spectrum Disorder ResearchGenetics and Neurodevelopmental DisordersNeuroendocrine regulation and behavior

The serotonin system in autism spectrum disorder: From biomarker to animal models

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Muller, C.L., Anacker, A.M.J., Veenstra-VanderWeele, J.·2016·Neuroscience

DOI 10.1016/j.neuroscience.2015.11.010PMC PMC4824539

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Abstract

Elevated whole blood serotonin, or hyperserotonemia, was the first biomarker identified in autism spectrum disorder (ASD) and is present in more than 25% of affected children. The serotonin system is a logical candidate for involvement in ASD due to its pleiotropic role across multiple brain systems both dynamically and across development. Tantalizing clues connect this peripheral biomarker with changes in brain and behavior in ASD, but the contribution of the serotonin system to ASD pathophysiology remains incompletely understood. Studies of whole blood serotonin levels in ASD and in a large founder population indicate greater heritability than for the disorder itself and suggest an association with recurrence risk. Emerging data from both neuroimaging and postmortem samples also indicate changes in the brain serotonin system in ASD. Genetic linkage and association studies of both whole blood serotonin levels and of ASD risk point to the chromosomal region containing the serotonin transporter (SERT) gene in males but not in females. In ASD families with evidence of linkage to this region, multiple rare SERT amino acid variants lead to a convergent increase in serotonin uptake in cell models. A knock-in mouse model of one of these variants, SERT Gly56Ala, recapitulates the hyperserotonemia biomarker and shows increased brain serotonin clearance, increased serotonin receptor sensitivity, and altered social, communication, and repetitive behaviors. Data from other rodent models also suggest an important role for the serotonin system in social behavior, in cognitive flexibility, and in sensory development. Recent work indicates that reciprocal interactions between serotonin and other systems, such as oxytocin, may be particularly important for social behavior. Collectively, these data point to the serotonin system as a prime candidate for treatment development in a subgroup of children defined by a robust, heritable biomarker.

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ASD-associated genes were enriched for acetylcholinergic and serotonergic signaling.
“ASD-associated genes were enriched for acetylcholinergic and serotonergic signaling, reflecting known biology of ASD20,21.”
From A computational tool (H-MAGMA) for improved prediction of brain-disorder risk genes by incorporating brain chromatin interaction profiles (2020) · cites this paper as [21]
Production of 5-HT can affect peripheral tryptophan availability and thus indirectly affect brain 5-HT levels, suggesting that peripheral alterations in 5-HT can affect the central 5-HT signaling system.
“Additionally, the production of 5-HT can affect peripheral tryptophan availability and, thus, indirectly affect brain 5-HT levels, suggesting that peripheral alterations in 5-HT can affect the central 5-HT signaling system (390, 391).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [390]
A number of biomarkers that could connect to microbial profiles have been identified in ASD, including alterations in serotonin levels, IL1β, and IL6.
“A number of biomarkers that could connect to microbial profiles also have been identified in ASD, including alterations in serotonin levels, IL1β, and IL6.35, 44, 45, 46, 47”
From Distinct Microbiome-Neuroimmune Signatures Correlate With Functional Abdominal Pain in Children With Autism Spectrum Disorder (2017) · cites this paper as [45]
Long-standing findings have indicated increased whole-blood 5-HT levels in a subset of approximately 30% of children with autism spectrum disorder.
“Long-standing findings have indicated increased whole-blood 5-HT levels in a subset of approximately 30% of children with autism spectrum disorder,44, 45, 46, 47 as well as decreased levels of the serotonin metabolite, melatonin, in a substantial subpopulation.62”
From Distinct Microbiome-Neuroimmune Signatures Correlate With Functional Abdominal Pain in Children With Autism Spectrum Disorder (2017) · cites this paper as [45]
Recent evidence suggests altered 5-HT and kynurenine metabolism in ASD.
“Of note, recent evidence suggests altered 5-HT and kynurenine metabolism in ASD (Boccuto et al., 2013; Lim et al., 2015; Muller et al., 2016).”
From Microbiota-related Changes in Bile Acid & Tryptophan Metabolism are Associated with Gastrointestinal Dysfunction in a Mouse Model of Autism (2017) · cites this paper as Muller et al., 2016

Most serotonin is produced in the GI tract and can be metabolized directly by the gut microbiota; it modulates neurodevelopment and might be important in social function and repetitive behavior.
“Although most serotonin, or 5′-HT, is produced in the GI tract and can also be metabolized directly by the gut microbiota, it modulates neurodevelopment and might be important in social function and repetitive behavior [188].”
From Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions (2019) · cites this paper as [188]
In patients with ASD, altered function and metabolism of neurotransmitters such as 5-HT and catecholamines, and dysfunction of the serotonergic system, have been reported to contribute to symptomatology.
“In patients with ASD, altered function and metabolism of neurotransmitters, such as 5′-HT and catecholamines, and dysfunction of the serotonergic system have been reported to contribute to symptomatology [188,192,193,194,195,196].”
From Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions (2019) · cites this paper as [188]
Approximately 30% of individuals with ASD exhibit an increase in whole-blood 5-HT levels, termed hyperserotonemia.
“studies revealed that approximately 30% of individuals with ASD exhibited an increase in whole-blood 5-HT levels, termed hyperserotonemia [35, 36].”
From Serotonin as a link between the gut-brain-microbiome axis in autism spectrum disorders (2018) · cites this paper as [36]
Five rare Slc6a4 variants overexpressed in individuals with ASD are gain-of-function mutations that confer hyperactivity to SERT.
“They identified five variants that were overexpressed in the individuals with ASD; each variant was a gain-of-function mutation that conferred a hyperactivity to SERT [36, 52].”
From Serotonin as a link between the gut-brain-microbiome axis in autism spectrum disorders (2018) · cites this paper as [36]
Clinical correlates between hyperserotonemia and ASD-associated behaviors (e.g., stereotypy and self-injury) have been inconsistent.
“the clinical correlates between hyperserotonemia and ASD-associated behaviors (e.g., stereotypy and self-injury) have been inconsistent [36, 45–47].”
From Serotonin as a link between the gut-brain-microbiome axis in autism spectrum disorders (2018) · cites this paper as [36]

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A Genomewide Screen of 345 Families for Autism-Susceptibility Loci
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Excessive Activation of Serotonin (5-HT) 1B Receptors Disrupts the Formation of Sensory Maps in Monoamine Oxidase A and 5-HT Transporter Knock-Out Mice
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Serotonin modulates the response of embryonic thalamocortical axons to netrin-1
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Social reward among juvenile mice
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Social approach in genetically engineered mouse lines relevant to autism
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A role for oxytocin and 5-HT1A receptors in the prosocial effects of 3,4 methylenedioxymethamphetamine (“ecstasy”)
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Oxytocin increases eye contact during a real-time, naturalistic social interaction in males with and without autism
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The evolution of the serotonergic nervous system
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Comparative Study of Pre- and Postsynaptic 5-HT1AReceptor Modulation of Anxiety in Two Ethological Animal Tests
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Hyperserotonemia and amine metabolites in autistic and retarded children
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A Double-Blind Placebo-Controlled Trial of Fluoxetine for Repetitive Behaviors and Global Severity in Adult Autism Spectrum Disorders
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Plasma oxytocin concentrations and OXTR polymorphisms predict social impairments in children with and without autism spectrum disorder
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“Biomarker and genetic data for OT and its receptor have been promising but inconsistent in ASD and in relation to various measures of human social behavior (Modahl et al., 1998, Jacob et al., 2007, Hammock et al., 2012, Miller et al., 2013a, Parker et al., 2014, Skuse et al., 2014).”
Background
Barrel Pattern Formation Requires Serotonin Uptake by Thalamocortical Afferents, and Not Vesicular Monoamine Release
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Common polymorphism in the oxytocin receptor gene ( OXTR ) is associated with human social recognition skills
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Serotonergic Responsivity in Male Young Adults With Autistic Disorder
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Oxytocin mediates early experience-dependent cross-modal plasticity in the sensory cortices
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Platelet serotonin levels in Pervasive Developmental Disorders and mental retardation: Diagnostic group differences, within-group distribution, and behavioral correlates
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Perinatal antidepressant exposure alters cortical network function in rodents
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Maternal administration of thalidomide or valproic acid causes abnormal serotonergic neurons in the offspring: implication for pathogenesis of autism
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Use of selective serotonin reuptake inhibitors during pregnancy and risk of autism
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Whole blood serotonin and plasma beta-endorphin in autistic probands and their first-degree relatives
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Pharmacological reduction of mucosal but not neuronal serotonin opposes inflammation in mouse intestine
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Oxytocin improves behavioural and neural deficits in inferring others’ social emotions in autism
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Autism and the serotonin transporter: the long and short of it
Devlin, B., Cook, E. H., Coon, H. H., Dawson, G., Grigorenko, E. L., McMahon, W., Minshew, N. J., Pauls, D. L., Smith, M., Spence, M. A., et al. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001724 · Cited by 187 · see citing works
Determination of serotonin in whole blood, platelet-rich plasma, platelet-poor plasma and plasma ultrafiltrate
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Cortical Serotonin 5-HT 2A Receptor Binding and Social Communication in Adults With Asperger’s Syndrome: An in Vivo SPECT Study
Murphy, D., Daly, E., Schmitz, N., Toal, F., Murphy, K., Curran, S. R., Erlandsson, K., Eersels, J. L. H., Kerwin, R. W., Ell, P. J., et al. (2006) · American Journal of Psychiatry · doi:10.1176/ajp.2006.163.5.934 · Cited by 181 · see citing works
Interactions between integrin αIIbβ3 and the serotonin transporter regulate serotonin transport and platelet aggregation in mice and humans
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Switching brain serotonin with oxytocin
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Evidence for Sex-Specific Risk Alleles in Autism Spectrum Disorder
Stone, J. L., Merriman, B., Cantor, R. M., Yonan, A. L., Gilliam, T. C., Geschwind, D. H., & Nelson, S. F. (2004) · The American Journal of Human Genetics · doi:10.1086/426034 · Cited by 176 · see citing works
Prenatal SSRI use and offspring with autism spectrum disorder or developmental delay
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Decreased tryptophan metabolism in patients with autism spectrum disorders
Boccuto, L., Chen, C., Pittman, A. R., Skinner, C. D., McCartney, H., Jones, K. A., Bochner, B. R., Stevenson, R. E., & Schwartz, C. E. (2013) · Molecular Autism · doi:10.1186/2040-2392-4-16 · Cited by 171 · see citing works
Serotonin and dopamine transporter binding in children with autism determined by SPECT
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Vesicular and Plasma Membrane Transporters for Neurotransmitters
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Behavior and serotonergic disorders in rats exposed prenatally to valproate: A model for autism
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Monoamine-sensitive developmental periods impacting adult emotional and cognitive behaviors
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Platelet serotonin studies in hyperserotonemic relatives of children with autistic disorder
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Effect of serotonin depletion on vibrissa-related patterns of thalamic afferents in the rat's somatosensory cortex
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The serotonin-N-acetylserotonin-melatonin pathway as a biomarker for autism spectrum disorders
Pagan, C., Delorme, R., Callebert, J., Goubran-Botros, H., Amsellem, F., Drouot, X., Boudebesse, C., Le Dudal, K., Ngo-Nguyen, N., Laouamri, H., et al. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.120 · Cited by 165 · see citing works
Broad and narrow heritabilities of quantitative traits in a founder population
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Evidence for epistasis between SLC6A4 and ITGB3 in autism etiology and in the determination of platelet serotonin levels
Coutinho, A. M., Sousa, I., Martins, M., Correia, C., Morgadinho, T., Bento, C., Marques, C., Ataíde, A., Miguel, T. S., Moore, J. H., et al. (2007) · Human Genetics · doi:10.1007/s00439-006-0301-3 · Cited by 153 · see citing works
Maternal Conditions and Perinatal Characteristics Associated with Autism Spectrum Disorder and Intellectual Disability
Langridge, A., Glasson, E. J., Nassar, N., Jacoby, P. A., Pennell, C. E., Hagan, R., Bourke, J., Leonard, H., & Stanley, F. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0050963 · Cited by 151 · see citing works
Oxytocin and Vasopressin in Children and Adolescents With Autism Spectrum Disorders: Sex Differences and Associations With Symptoms
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Haploinsufficiency for Pten and Serotonin transporter cooperatively influences brain size and social behavior
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Platelet serotonin, a possible marker for familial autism
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Serotonin Mediates Cross-Modal Reorganization of Cortical Circuits
Jitsuki, S., Takemoto, K., Kawasaki, T., Tada, H., Takahashi, A., Bécamel, C., Sano, A., Yuzaki, M., Zukin, R. S., Ziff, E. B., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.016 · Cited by 145 · see citing works
Postnatal Day 2 to 11 Constitutes a 5-HT-Sensitive Period Impacting Adult mPFC Function
Rebello, T. J., Yu, Q., Goodfellow, N. M., Cagliostro, M. K. C., Teissier, A., Morelli, E., Demireva, E. Y., Chemiakine, A., Rosoklija, G. B., Dwork, A. J., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1020-13.2014 · Cited by 143 · see citing works
Mice Genetically Depleted of Brain Serotonin Display Social Impairments, Communication Deficits and Repetitive Behaviors: Possible Relevance to Autism
Kane, M. J., Angoa‐Pérez, M., Briggs, D. I., Sykes, C. E., Francescutti, D. M., Rosenberg, D. R., & Kuhn, D. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048975 · Cited by 143 · see citing works
Autism spectrum disorder severity reflects the average contribution of de novo and familial influences
Robinson, E. B., Samocha, K. E., Kosmicki, J. A., McGrath, L., Neale, B. M., Perlis, R. H., & Daly, M. J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1409204111 · Cited by 142 · see citing works
Effects of Diagnosis, Race, and Puberty on Platelet Serotonin Levels in Autism and Mental Retardation
MCBRIDE, P. A., ANDERSON, G. M., HERTZIG, M. E., SNOW, M. E., THOMPSON, S. M., KHAIT, V. D., SHAPIRO, T., & COHEN, D. J. (1998) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-199807000-00017 · Cited by 141 · see citing works
Scheduling of Monoaminergic Neurotransmitter Receptor Expression in the Primate Neocortex during Postnatal Development
Lidow, M. S., & Rakic, P. (1992) · Cerebral Cortex · doi:10.1093/cercor/2.5.401 · Cited by 141 · see citing works
Postnatal development of serotonin nerve fibers in the somatosensory cortex of mice studied by immunohistochemistry
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Density and function of central serotonin (5-HT) transporters, 5-HT1A and 5-HT2A receptors, and effects of their targeting on BTBR T+tf/J mouse social behavior
Gould, G. G., Hensler, J. G., Burke, T. F., Benno, R. H., Onaivi, E. S., & Daws, L. C. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.07104.x · Cited by 138 · see citing works
Excess of serotonin affects embryonic interneuron migration through activation of the serotonin receptor 6
Riccio, O., Potter, G., Walzer, C., Vallet, P., Szabó, G., Vutskits, L., Kiss, J. Z., & Dayer, A. G. (2008) · Molecular Psychiatry · doi:10.1038/mp.2008.89 · Cited by 138 · see citing works
Sex-specific genetic architecture of whole blood serotonin levels
Weiss, L. A., Abney, M., Cook, E. H., & Ober, C. (2005) · The American Journal of Human Genetics · doi:10.1086/426697 · Cited by 137 · see citing works
Linkage and association analysis at the serotonin transporter (SLC6A4) locus in a rigid‐compulsive subset of autism
McCauley, J. L., Olson, L. M., Dowd, M., Amin, T. T., Steele, A., Blakely, R., Folstein, S. E., Haines, J. L., & Sutcliffe, J. S. (2003) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.20151 · Cited by 136 · see citing works
Variants of the serotonin transporter gene (SLC6A4) significantly contribute to hyperserotonemia in autism
Coutinho, A. M., Oliveira, G. G., Morgadinho, T., Fesel, C., Macedo, T. R. A., Bento, C., Marques, C., Ataíde, A., Miguel, T., Borges, L., et al. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001409 · Cited by 136 · see citing works
Enhancement of Spatial Reversal Learning by 5-HT2CReceptor Antagonism Is Neuroanatomically Specific
Boulougouris, V., & Robbins, T. W. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4312-09.2010 · Cited by 136 · cited 1× · see citing works
“Drugs targeting serotonin receptors, particularly 5-HT1A and 5-HT2A, have shown promise for increasing social interaction or decreasing cognitive rigidity (File et al., 1996, Edwards et al., 2006, Boulougouris and Robbins, 2010, Gould et al., 2011, Amodeo et al., 2014).”
Background
Serotonin transporter promoter variants in autism: functional effects and relationship to platelet hyperserotonemia
Anderson, G. M., Gutknecht, L., Cohen, D. J., Brailly‐Tabard, S., Cohen, J. H. M., Ferrari, P., Roubertoux, P. L., & Tordjman, S. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001099 · Cited by 127 · see citing works
Enhanced activity of human serotonin transporter variants associated with autism
Prasad, H. C., Steiner, J. A., Sutcliffe, J. S., & Blakely, R. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0143 · Cited by 126 · see citing works
Elevated blood serotonin in autistic probands and their first-degree relatives
Abramson, R. K., Wright, H. H., Carpenter, R., Brennan, W., Lumpuy, O., Cole, E., & Young, S. R. (1989) · Journal of Autism and Developmental Disorders · doi:10.1007/bf02212938 · Cited by 123 · see citing works
Monoamine oxidase A and A/B knockout mice display autistic-like features
Bortolato, M., Godar, S. C., Alzghoul, L., Zhang, J., Darling, R. D., Simpson, K. L., Bini, V., Chen, K., Wellman, C. L., Lin, R. C. S., et al. (2012) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712000715 · Cited by 118 · see citing works
Expression mapping of 5-HT1 serotonin receptor subtypes during fetal and early postnatal mouse forebrain development
Bonnin, A., Peng, W., Hewlett, W., & Levitt, P. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.036 · Cited by 117 · see citing works
Oxytocin and Autism: A Systematic Review of Randomized Controlled Trials
Preti, A., Melis, M., Siddi, S., Vellante, M., Doneddu, G., & Fadda, R. (2014) · Journal of Child and Adolescent Psychopharmacology · doi:10.1089/cap.2013.0040 · Cited by 114 · see citing works
Absence of preference for social novelty and increased grooming in integrin β3 knockout mice: Initial studies and future directions
Carter, M. D., Shah, C. R., Muller, C. L., Crawley, J. N., Carneiro, A. M. D., & Veenstra-VanderWeele, J. M. (2011) · Autism Research · doi:10.1002/aur.180 · Cited by 112 · see citing works
Self-citation
Reduced fear and aggression and altered serotonin metabolism in Gtf2ird1‐targeted mice
Young, E. J., Lipina, T. V., Tam, E., Mandel, A., Clapcote, S. J., Bechard, A. R., Chambers, J., Mount, H. T. J., Fletcher, P. J., Roder, J., et al. (2007) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2007.00343.x · Cited by 109 · see citing works
Increased serotonin axons (immunoreactive to 5-HT transporter) in postmortem brains from young autism donors
Azmitia, E. C., Singh, J. S., & Whitaker-Azmitia, P. M. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.02.002 · Cited by 107 · see citing works
Further studies in the developmental hyperserotonemia model (DHS) of autism: Social, behavioral and peptide changes
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Fluoxetine but not risperidone increases sociability in the BTBR mouse model of autism
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Anderson GM Feibel FC Cohen DJ 1987b Determination of serotonin in whole blood, platelet-rich plasma, platelet-poor plasma and plasma ultrafiltrate Life sciences 40 1063 1070 3821372
Cook EH Jr Arora RC Anderson GM Berry-Kravis EM Yan SY Yeoh HC Sklena PJ Charak DA Leventhal BL 1993b Platelet serotonin studies in hyperserotonemic relatives of children with autistic disorder Life sciences 52 2005 2015 7684805
Hanley HG Stahl SM Freedman DX 1977b Hyperserotonemia and amine metabolites in autistic and retarded children Arch Gen Psychiatry 34 521 531 860890
Weiss LA Veenstra-Vanderweele J Newman DL Kim SJ Dytch H McPeek MS Cheng S Ober C Cook EH Jr Abney M 2004b Genome-wide association study identifies ITGB3 as a QTL for whole blood serotonin Eur J Hum Genet 12 949 954 15292919

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“…of these studies is reinforced by the fact that serotonin has been consistently implicated in ASD [Cook & Leventhal, 1996; Mulder et al., 2004; Muller et al., 2016], has been shown to be important for sensory cortical development [Cases et al., 1996; Gaspar, Cases, & Maroteaux, 2003; Salichon…”
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Authors: Muller, C. L., Anacker, A. M. J., & Veenstra-VanderWeele, J.
Affiliations: Vanderbilt University (US)
Columbia University (US)
NewYork–Presbyterian Hospital (US)
Corresponding author: Veenstra-VanderWeele, J.
ORCID: Veenstra-VanderWeele, J.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 2016-05
Volume: 321
Pages: 24-41
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/j.neuroscience.2015.11.010
PMC: PMC4824539
OpenAlex: W2119744351
Cited by: 531
References: 236
Citations by year: 2026: 54 · 2025: 44 · 2024: 55 · 2023: 60 · 2022: 50 · 2021: 63 · 2020: 59 · 2019: 48 · 2018: 45 · 2017: 33 · 2016: 18 · 2015: 1 · 2013: 1
FWCI: 3.21
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: NIH (MH094604)
New York State Psychiatric Institute
Mortimer D. Sackler Chair Fund
Columbia University
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords: autism spectrum disorder, serotonergic system, hyperserotonemia, whole blood serotonin, serotonin transporter gene, knock-in mice, heritability, recurrence risk, serotonin receptors, social behavior, oxytocin, cognitive flexibility, sensory development, ASD pathophysiology
MeSH terms: Autism Spectrum Disorder, Animals, Brain, Disease Models, Animal, Female, Humans, Genetic Linkage, Male, Mice, Mutant Strains, Serotonin, Sex Factors, Biomarkers, Serotonin Plasma Membrane Transport Proteins, Genetic Association Studies

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