ArticleBiological psychiatry2019
Habituation Learning Is a Widely Affected Mechanism in Drosophila Models of Intellectual Disability and Autism Spectrum Disorders.
Article in Biological psychiatry, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 32 papers.
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32 citing papers in PubMed, 66 citations in OpenAlex.
- Nighttime sleep promotes mechanosensory habituation inbioRxiv : the preprint server for biology · 2026Article
- Dynamical modeling of individual sensory reactivity and habituation learning.Proceedings of the National Academy of Sciences of the United States of America · 2026Article
- Pre-Pulse Inhibition of an escape response in adult fruit fly, Drosophila melanogaster.Translational psychiatry · 2026Article
- Infant sensory gating and a developmental cascade to autistic traits and anxiety.Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology · 2026Review
- Neurofibromin Deficiency Alters the Patterning and Prioritization of Motor Behaviors in a State-Dependent Manner.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2025Article
- Sex-Specific Effects of Social Environment on Behaviour and Their Correlations inEcology and evolution · 2025Article
- Biallelic variants in GTF3C3 result in an autosomal recessive disorder with intellectual disability.Genetics in medicine : official journal of the American College of Medical Genetics · 2025Article
- Neurofibromin deficiency alters the patterning and prioritization of motor behaviors in a state-dependent manner.bioRxiv : the preprint server for biology · 2024Article
- KDM5-mediated transcriptional activation of ribosomal protein genes alters translation efficiency to regulate mitochondrial metabolism in neurons.Nucleic acids research · 2024Article
- Review
- Strategies for dissecting the complexity of neurodevelopmental disorders.Trends in genetics : TIG · 2024Review
- The ortholog of human ssDNA-binding protein SSBP3 influences neurodevelopment and autism-like behaviors in Drosophila melanogaster.PLoS biology · 2023Article
- Article
- Review
- Loss ofThe Journal of neuroscience : the official journal of the Society for Neuroscience · 2022Article
- Intellectual disability-associated disruption of O-GlcNAc cycling impairs habituation learning in Drosophila.PLoS genetics · 2022Article
- Prenatal ethanol exposure impairs sensory processing and habituation to visual stimuli, effects normalized by enrichment of postnatal environmental.Alcoholism, clinical and experimental research · 2022Article
- Rapid assessment of the temporal function and phenotypic reversibility of neurodevelopmental disorder risk genes in Caenorhabditis elegans.Disease models & mechanisms · 2022Article
- Germline variants in tumor suppressor FBXW7 lead to impaired ubiquitination and a neurodevelopmental syndrome.American journal of human genetics · 2022Article
- Impact of brain overgrowth on sensorial learning processing during the first year of life.Frontiers in human neuroscience · 2022Article
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14 authors at 6 institutions in 5 countries.
Funding
Abstract
backgroundAlthough habituation is one of the most ancient and fundamental forms of learning, its regulators and its relevance for human disease are poorly understood.
methodsWe manipulated the orthologs of 286 genes implicated in intellectual disability (ID) with or without comorbid autism spectrum disorder (ASD) specifically in Drosophila neurons, and we tested these models in light-off jump habituation. We dissected neuronal substrates underlying the identified habituation deficits and integrated genotype-phenotype annotations, gene ontologies, and interaction networks to determine the clinical features and molecular processes that are associated with habituation deficits.
resultsWe identified >100 genes required for habituation learning. For 93 of these genes, a role in habituation learning was previously unknown. These genes characterize ID disorders with macrocephaly and/or overgrowth and comorbid ASD. Moreover, individuals with ASD from the Simons Simplex Collection carrying damaging de novo mutations in these genes exhibit increased aberrant behaviors associated with inappropriate, stereotypic speech. At the molecular level, ID genes required for normal habituation are enriched in synaptic function and converge on Ras/mitogen-activated protein kinase (Ras/MAPK) signaling. Both increased Ras/MAPK signaling in gamma-aminobutyric acidergic (GABAergic) neurons and decreased Ras/MAPK signaling in cholinergic neurons specifically inhibit the adaptive habituation response.
conclusionsOur work supports the relevance of habituation learning to ASD, identifies an unprecedented number of novel habituation players, supports an emerging role for inhibitory neurons in habituation, and reveals an opposing, circuit-level-based mechanism for Ras/MAPK signaling. These findings establish habituation as a possible, widely applicable functional readout and target for pharmacologic intervention in ID/ASD.
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