Malformation of the superior olivary complex in an animal model of autism
Abstract
Autism is a neurodevelopmental disorder characterized by social difficulties, impaired communication skills and repetitive behavioral patterns. Additionally, there is evidence that auditory deficits are a common feature of the autism spectrum disorders. Despite the prevalence of autism, the neurobiology of this disorder is poorly understood. However, abnormalities in neuronal morphology, cell number and connectivity have been described throughout the autistic brain. Indeed, we have demonstrated significant dysmorphology in the superior olivary complex (SOC), a collection of auditory brainstem nuclei, in the autistic brain. Prenatal exposure to valproic acid (VPA) in humans has been associated with autism and in rodents prenatal VPA exposure produces many neuroanatomical and behavioral deficits associated with autism. Thus, in an effort to devise an animal model of the autistic auditory brainstem, we have investigated neuronal number and morphology in animals prenatally exposed to valproic acid (VPA). In VPA exposed rats, we find significantly fewer neurons and significant alterations in neuronal morphology. Thus, prenatal VPA exposure in rats appears to produce similar dysmorphology as we have reported in the autistic human brain.
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Following prenatal VPA exposure, cell density is increased in the hippocampus but decreased in the cerebellum and the superior olivary nuclei of the brainstem.
“Cell density is increased in the hippocampus [94], but it is decreased in the cerebellum [164] and the superior olivary nuclei of the brainstem [221] following prenatal VPA exposure.”
From Autism spectrum disorder: neuropathology and animal models (2017) · cites this paper as [221]
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Autism spectrum disorder: neuropathology and animal models
Varghese, M., Keshav, N., Jacot-Descombes, S., Warda, T., Wicinski, B., Dickstein, D. L., Harony-Nicolas, H., De Rubeis, S., Drapeau, E., Buxbaum, J. D., et al. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1736-4 · Cited by 536 · see citing works
Williams, Z. J., He, J. L., Cascio, C. J., & Woynaroski, T. G. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.11.030 · Cited by 175 · see citing works
Lauber, E., Filice, F., & Schwaller, B. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2016.00150 · Cited by 90 · see citing works
Autism Traits in Individuals with Agenesis of the Corpus Callosum
Lau, Y. C., Hinkley, L. B. N., Bukshpun, P., Strominger, Z. A., Wakahiro, M. L. J., Baron‐Cohen, S., Allison, C. L., Bonnie Auyeung, B., Jeremy, R. J., Nagarajan, S. S., et al. (2012) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-012-1653-2 · Cited by 89 · see citing works
Repeated prenatal exposure to valproic acid results in cerebellar hypoplasia and ataxia
Main, S. L., & Kulesza, R. J. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2016.10.052 · Cited by 80 · see citing works
Self-citationDeletion of Fmr1 alters function and synaptic inputs in the auditory brainstem
Rotschafer, S. E., Marshak, S., & Cramer, K. S. (2015) · PLOS ONE · doi:10.1371/journal.pone.0117266 · Cited by 72 · see citing works
Evidence for Brainstem Contributions to Autism Spectrum Disorders
Dadalko, O. I., & Travers, B. G. (2018) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2018.00047 · Cited by 66 · see citing works
Engineer, C. T., Centanni, T. M., Im, K. W., Borland, M. S., Moreno, N. A., Carraway, R. S., Wilson, L. G., & Kilgard, M. P. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22175 · Cited by 55 · see citing works
A Systematic Review of Brainstem Contributions to Autism Spectrum Disorder
Seif, A., Shea, C., Schmid, S., & Stevenson, R. A. (2021) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2021.760116 · Cited by 54 · see citing works
Zimmerman, R., Patel, R., Smith, A., Pasos, J., & Kulesza, R. J. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.02.030 · Cited by 42 · see citing works
Self-citationCentral Auditory and Vestibular Dysfunction Are Key Features of Autism Spectrum Disorder
Mansour, Y., Burchell, A., & Kulesza, R. J. (2021) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2021.743561 · Cited by 41 · see citing works
Self-citationTime-dependent Gene Expression Analysis of the Developing Superior Olivary Complex
Ehmann, H., Hartwich, H., Salzig, C. P. J., Hartmann, N., Clément‐Ziza, M., Ushakov, K., Avraham, K. B., Bininda‐Emonds, O. R. P., Hartmann, A. K., Lang, P. M., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.490508 · Cited by 37 · see citing works
Zimmerman, R., Smith, A., Fech, T., Mansour, Y., & Kulesza, R. J. (2020) · Experimental Brain Research · doi:10.1007/s00221-020-05729-7 · Cited by 37 · see citing works
Self-citationAuditory Midbrain Hypoplasia and Dysmorphology after Prenatal Valproic Acid Exposure
Mansour, Y., Mangold, S., Chosky, D., & Kulesza, R. J. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.11.016 · Cited by 36 · see citing works
Self-citationPrenatal valproic acid exposure disrupts tonotopic c-Fos expression in the rat brainstem
Dubiel, A., & Kulesza, R. J. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.10.043 · Cited by 35 · see citing works
Self-citationMansour, Y., Ahmed, S. N., & Kulesza, R. J. (2020) · Experimental Brain Research · doi:10.1007/s00221-020-05982-w · Cited by 32 · see citing works
Self-citationDevelopmental Emergence of Phenotypes in the Auditory Brainstem Nuclei ofFmr1Knockout Mice
Rotschafer, S. E., & Cramer, K. S. (2017) · eNeuro · doi:10.1523/eneuro.0264-17.2017 · Cited by 30 · see citing works
Degraded cortical temporal processing in the valproic acid-induced rat model of autism
Cheng, Y., Tang, B., Zhang, G., An, P., Sun, Y., Gao, M. Z., Zhang, Y., Shan, Y., Zhang, J., Liu, Q., et al. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109000 · Cited by 30 · see citing works
Auditory Dysfunction in Animal Models of Autism Spectrum Disorder
Castro, A. C., & Monteiro, P. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.845155 · Cited by 34 · see citing works
Gottfried, C., Bambini-Júnior, V., Baronio, D., Zanatta, G., Bristot, R., Vaccaro, T. D. S., & Riesgo, R. D. S. (2013) · InTech eBooks · doi:10.5772/54824 · Cited by 28 · see citing works
Auditory Brainstem Pathology in Autism Spectrum Disorder: A Review
Pillion, J. P., Boatman‐Reich, D., & Gordon, B. (2018) · Cognitive and Behavioral Neurology · doi:10.1097/wnn.0000000000000154 · Cited by 27 · see citing works
Foran, L. A., Blackburn, K., & Kulesza, R. J. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.01.004 · Cited by 25 · see citing works
Self-citationCharacterization of the human central nucleus of the inferior colliculus
Mansour, Y., Altaher, W., & Kulesza, R. J. (2019) · Hearing Research · doi:10.1016/j.heares.2019.04.004 · Cited by 24 · see citing works
Self-citationPrenatal valproic acid exposure disrupts tonotopic c-Fos expression in the rat brainstem
Dubiel, A., & Kulesza, R. J. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.01.030 · Cited by 22 · see citing works
Self-citationAbnormal auditory brainstem responses in an animal model of autism spectrum disorder.
Malhotra, A., & Kulesza, R. (2023) · Hearing Research · doi:10.1016/j.heares.2023.108816 · Cited by 14 · see citing works
Self-citationMechanism of auditory hypersensitivity in human autism using autism model rats
Ida‐Eto, M., Hara, N., Ohkawara, T., & Narita, M. (2016) · Pediatrics International · doi:10.1111/ped.13186 · Cited by 21 · see citing works
Wei, R., Li, Q., Lam, S., Leung, J., Cheung, C., Zhang, X., Sham, P. C., Chua, S. E., & McAlonan, G. M. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.08.006 · Cited by 18 · see citing works
Abnormal vestibular brainstem structure and function in an animal model of autism spectrum disorder
Mansour, Y., Burchell, A., & Kulesza, R. J. (2022) · Brain Research · doi:10.1016/j.brainres.2022.148056 · Cited by 16 · see citing works
Self-citationRecent advances in animal model experimentation in autism research
Tania, M., Khan, M. A., & Xia, K. (2013) · Acta Neuropsychiatrica · doi:10.1017/neu.2013.58 · Cited by 16 · see citing works
Prenatal Exposure to Valproate in Animals and Autism
Bambini-Júnior, V., Baronio, D., MacKenzie, J., Zanatta, G., Riesgo, R. D. S., & Gottfried, C. (2013) · Springer eBooks · doi:10.1007/978-1-4614-4788-7_108 · Cited by 14 · see citing works
Korn, M. J., Koppel, S. J., & Cramer, K. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027383 · Cited by 13 · see citing works
Research progress of the inferior colliculus: from Neuron, neural circuit to auditory disease
Liu, M., Wang, Y., Jiang, L., Zhang, X., Wang, C., & Zhang, T. (2024) · Brain Research · doi:10.1016/j.brainres.2024.148775 · Cited by 11 · see citing works
Anshu, K., Nair, A. K., Srinath, S., & Laxmi, T. R. (2022) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-022-05684-y · Cited by 12 · see citing works
Characterization of the superior olivary complex of Canis lupus domesticus
Fech, T., Calderón‐Garcidueñas, L., & Kulesza, R. J. (2017) · Hearing Research · doi:10.1016/j.heares.2017.06.010 · Cited by 10 · see citing works
Self-citationKosmer, K., & Kulesza, R. J. (2024) · Cerebral Cortex · doi:10.1093/cercor/bhad501 · Cited by 10 · see citing works
Self-citationDegraded inferior colliculus responses to complex sounds in prenatally exposed VPA rats
Tamaoki, Y., Pasapula, V., Chandler, C., Borland, M. S., Olajubutu, O. I., Tharakan, L. S., & Engineer, C. T. (2024) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-023-09514-9 · Cited by 8 · see citing works
Rahdar, M., Hajisoltani, R., Davoudi, S., Karimi, S. A., Borjkhani, M., Khatibi, V. A., Hosseinmardi, N., Behzadi, G., & Janahmadi, M. (2022) · Brain Research · doi:10.1016/j.brainres.2022.148013 · Cited by 8 · see citing works
Tsugiyama, L. E., Ida‐Eto, M., Ohkawara, T., Noro, Y., & Narita, M. (2019) · Congenital Anomalies · doi:10.1111/cga.12353 · Cited by 8 · see citing works
Chauhan, V. P. S., & Chauhan, A. (2014) · Oxidative stress in applied basic research and clinical practice · doi:10.1007/978-1-4939-0440-2_4 · Cited by 7 · see citing works
Medial superior olive in the rat: Anatomy, sources of input and axonal projections
Rincón, H., Gómez-Martínez, M., Gómez‐Álvarez, M., & Saldaña, E. (2024) · Hearing Research · doi:10.1016/j.heares.2024.109036 · Cited by 6 · see citing works
Alhelo, H., & Kulesza, R. J. (2021) · Folia Morphologica · doi:10.5603/fm.a2021.0098 · Cited by 5 · see citing works
Self-citationThe Superior Paraolivary Nucleus
Magnusson, A. K., & Gómez‐Álvarez, M. (2018) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190849061.013.11 · Cited by 5 · see citing works
Samy, K. L., Osman, D. M., Selim, M. H., & Mohamed, R. A. (2012) · The Egyptian Journal of Otolaryngology · doi:10.7123/01.ejo.0000413494.24410.1f · Cited by 4 · see citing works
Cacciato‐Salcedo, S., Lao-Rodríguez, A. B., & Malmierca, M. S. (2026) · Communications Biology · doi:10.1038/s42003-026-09585-z · Cited by 4 · see citing works
Obliteration of a glycinergic projection to the medial geniculate in an animal model of autism
Mansour, Y., & Kulesza, R. J. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1465255 · Cited by 2 · see citing works
Self-citationAlhelo, H., Dogiparthi, J., Baizer, J. S., Hof, P. R., Sherwood, C. C., & Kulesza, R. J. (2023) · Hearing Research · doi:10.1016/j.heares.2023.108698 · Cited by 2 · see citing works
Self-citationCacciato‐Salcedo, S., Lao-Rodríguez, A. B., & Malmierca, M. S. (2025) · Autism Research · doi:10.1002/aur.70125 · Cited by 1 · see citing works
Cacciato‐Salcedo, S., Lao-Rodríguez, A. B., & Malmierca, M. S. (2025) · Hearing Research · doi:10.1016/j.heares.2025.109470 · Cited by 1 · see citing works
Ratree, F., Franco, S., & Kulesza, R. J. (2026) · Hearing Research · doi:10.1016/j.heares.2026.109656 · Cited by 1 · see citing works
Self-citationAutism Traits in Individuals with Agenesis of the Corpus
Lau, Y., Nagarajan, H. S. S., Marco, E. J., Strominger, Z. A., Baron‐Cohen, S., Allison, C., Bonnie Auyeung, B., & Jeremy, R. J. (2012) · Cited by 1 · see citing works
Tamaoki, Y., Pasapula, V., Chandler, C., Borland, M. S., Olajubutu, O. I., Tharakan, L. S., & Engineer, C. T. (2024) · Figshare · doi:10.6084/m9.figshare.26658199
Tamaoki, Y., Pasapula, V., Chandler, C., Borland, M. S., Olajubutu, O. I., Tharakan, L. S., & Engineer, C. T. (2024) · Figshare · doi:10.6084/m9.figshare.26658205
Tamaoki, Y., Pasapula, V., Chandler, C., Borland, M. S., Olajubutu, O. I., Tharakan, L. S., & Engineer, C. T. (2024) · Figshare · doi:10.6084/m9.figshare.26658202
Tamaoki, Y., Pasapula, V., Chandler, C., Borland, M. S., Olajubutu, O. I., Tharakan, L. S., & Engineer, C. T. (2024) · Figshare · doi:10.6084/m9.figshare.24934372
Tamaoki, Y., Pasapula, V., Chandler, C., Borland, M. S., Olajubutu, O. I., Tharakan, L. S., & Engineer, C. T. (2024) · Figshare · doi:10.6084/m9.figshare.26658208
Tamaoki, Y., Pasapula, V., Chandler, C., Borland, M. S., Olajubutu, O. I., Tharakan, L. S., & Engineer, C. T. (2024) · Figshare · doi:10.6084/m9.figshare.26658196
Tamaoki, Y., Pasapula, V., Chandler, C., Borland, M. S., Olajubutu, O. I., Tharakan, L. S., & Engineer, C. T. (2024) · Figshare · doi:10.6084/m9.figshare.24934549
Vestibular brainstem impairment following in utero exposure to high dose paracetamol
Graeca, M., Donnelly, A., Cain, L., & Kulesza, R. J. (2026) · Brain Research · doi:10.1016/j.brainres.2026.150282
Self-citationVarman, D. R., Martínez‐Torres, A., Gutiérrez-Alvarado, M. E., Arellano, R. O., & Reyes‐Haro, D. (2026) · Future Pharmacology · doi:10.3390/futurepharmacol6030046
- Authors
- Lukose, R., Schmidt, E., Wolski, T. P., Murawski, N. J., & Kulesza, R. J.
- Affiliations
- UPMC Hamot (US)
- Lake Erie College of Osteopathic Medicine (US)
- University of Delaware (US)
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 2011-06
- Volume
- 1398
- Pages
- 102-112
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2022217727
- Cited by
- 59
- References
- 106
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 12 · 2023: 2 · 2022: 5 · 2021: 3 · 2020: 3 · 2019: 2 · 2018: 5 · 2017: 4 · 2016: 5 · 2015: 2 · 2014: 2 · 2013: 4 · 2012: 3
- FWCI
- 1.62
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
- Keywords
- autism spectrum disorder, superior olivary complex, valproic acid, prenatal drug exposure, auditory brainstem, neuronal morphology, neuron number, animal models of autism, auditory deficits
- MeSH terms
- Animals, Auditory Pathways, Auditory Perceptual Disorders, Autistic Disorder, Disease Models, Animal, Female, Language Development Disorders, Olivary Nucleus, Pregnancy, Valproic Acid, Rats
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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