Embryological exposure to valproic acid disrupts morphology of the deep cerebellar nuclei in a sexually dimorphic way

Mowery, Todd M.; Wilson, Sarah M.; Kostylev, Polina V.; Dina, Blair; Buchholz, Jennifer B.; Prieto, Anne L.; Garraghty, Preston E.

doi:10.1016/j.ijdevneu.2014.10.003

Cited by 29Autism Spectrum Disorder ResearchGenetics and Neurodevelopmental DisordersPharmacological Effects and Toxicity Studies

Embryological exposure to valproic acid disrupts morphology of the deep cerebellar nuclei in a sexually dimorphic way

Mowery, Todd M., Wilson, Sarah M., Kostylev, Polina V., Dina, Blair, Buchholz, Jennifer B., Prieto, Anne L., Garraghty, Preston E.·2015·International Journal of Developmental Neuroscience

DOI 10.1016/j.ijdevneu.2014.10.003

Open this paper in CoChat — free account

Abstract

Autism spectrum disorders (ASD) is diagnosed in males at a much higher rate than females. For this reason, the majority of autism research has used male subjects exclusively. However; more recent studies using genetic sex as a factor find that the development of the male and female brain is differentially affected by ASD. That is, the natural sex‐specific differences that exist between male and female brains lead to sexually dimorphic expressions of autism. Here we investigate the putative sexual dimorphism that exists in the deep cerebellar nuclei of male and female rats exposed to valproic acid (VPA) on embryological day 12.5. We find natural sex‐specific differences in adult nucleus area, length, and estimated cell populations. Therefore VPA exposure during embryology creates some sex‐specific deficits such as higher cell counts in the VPA males and lower cell counts in the VPA females. At the same time, some effects of VPA exposure occur regardless of sex. That is, smaller nucleus area and length lead to truncated nuclei in both VPA males and females. These deficits are more pronounced in the VPA males suggesting that genetic sex could play a role in teratogenic susceptibility to VPA. Taken together our results suggests that VPA exposure induces sexually dimorphic aberrations in morphological development along a mediolateral gradient at a discrete region of the hindbrain approximate to rhombomere (R) 1 and 2. Sex‐specific disruption of the local and long‐range projections emanating from this locus of susceptibility could offer a parsimonious explanation for the brain‐wide neuroanatomical variance reported in males and females with ASD.

Integrity signals

Registry

Crossref · 10.1016/j.ijdevneu.2014.10.003

Cites

90 of 90 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

In prenatal VPA models, the cerebellum decreases in size and the amygdala increases in size.
“Other brain areas that are affected include the cerebellum which decreases in size [247], and the amygdala which increases in size [265].”
From Autism spectrum disorder: neuropathology and animal models (2017) · cites this paper as [247]

Diagnostic and Statistical Manual of Mental Disorders
Williams, J. B. W., & First, M. B. (2013) · Oxford University Press eBooks · doi:10.1093/acrefore/9780199975839.013.104 · Cited by 109,841 · see citing works
The empathy quotient: an investigation of adults with asperger syndrome or high functioning autism, and normal sex differences
Baron-Cohen, S., & Wheelwright, S. (2004) · Journal of Autism and Developmental Disorders · doi:10.1023/b:jadd.0000022607.19833.00 · Cited by 4,093 · see citing works
The extreme male brain theory of autism
Baron-Cohen, S. (2002) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(02)01904-6 · Cited by 2,007 · see citing works
Cerebellum and nonmotor function
Strick, P. L., Dum, R. P., & Fiez, J. A. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125606 · Cited by 1,777 · see citing works
Epidemiological Surveys of Autism and Other Pervasive Developmental Disorders: An Update
Fombonne, E. (2003) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1025054610557 · Cited by 1,505 · see citing works
Neuroanatomy of autism
Amaral, D. G., Schumann, C. M., & Nordahl, C. W. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2007.12.005 · Cited by 1,492 · see citing works
The Extreme Male-Brain Theory of Autism
Baron‐Cohen, S. (1999) · The MIT Press eBooks · doi:10.7551/mitpress/4945.003.0023 · Cited by 1,413 · see citing works
Diagnostic and Statistical Manual of Mental Disorders
(2018) · Sage eBooks · doi:10.4135/9781506326139.n198 · Cited by 1,243 · see citing works
Sex differences in the brain: implications for explaining autism
Baron-Cohen, S., Knickmeyer, R. C., & Belmonte, M. K. (2005) · Science · doi:10.1126/science.1115455 · Cited by 1,145 · see citing works
Hypoplasia of cerebellar vermal lobules VI and VII in autism
Courchesne, E., Yeung-Courchesne, R., Hesselink, J. R., & Jernigan, T. L. (1988) · New England Journal of Medicine · doi:10.1056/nejm198805263182102 · Cited by 1,058 · see citing works
The epidemiology of autism: a review
FOMBONNE, E. (1999) · Psychological Medicine · doi:10.1017/s0033291799008508 · Cited by 981 · see citing works
Histoanatomic observations of the brain in early infantile autism
Bauman, M., & Kemper, T. L. (1985) · Neurology · doi:10.1212/wnl.35.6.866 · Cited by 964 · see citing works
Birth defects after maternal exposure to corticosteroids: Prospective cohort study and meta-analysis of epidemiological studies
Park‐Wyllie, L. Y., Mazzotta, P., Pastuszak, A. L., Moretti, M. E., Béïque, L. C., Hunnisett, L., Friesen, M. H., Jacobson, S., Kasapinovic, S., Chang, D., et al. (2000) · Teratology · doi:10.1002/1096-9926(200012)62:6 · Cited by 939 · see citing works
The systemizing quotient: an investigation of adults with Asperger syndrome or high–functioning autism, and normal sex differences
Baron-Cohen, S., Richler, J., Bisarya, D., Gurunathan, N., & Wheelwright, S. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1206 · Cited by 870 · see citing works
A behavioral comparison of male and female adults with high functioning autism spectrum conditions
Lai, M.-C., Lombardo, M. V., Pasco, G., Ruigrok, A. N. V., Wheelwright, S. J., Sadek, S. A., Chakrabarti, B., MRC AIMS Consortium, & Baron-Cohen, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020835 · Cited by 650 · see citing works
Lower Purkinje cell counts in the cerebella of four autistic subjects: initial findings of the UCLA-NSAC Autopsy Research Report
(1986) · American Journal of Psychiatry · doi:10.1176/ajp.143.7.862 · Cited by 590 · see citing works
The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy
Schmahmann, J. D. (2010) · Neuropsychology Review · doi:10.1007/s11065-010-9142-x · Cited by 583 · see citing works
Neural plate patterning: Upstream and downstream of the isthmic organizer
Wurst, W., & Bally‐Cuif, L. (2001) · Nature reviews. Neuroscience · doi:10.1038/35053516 · Cited by 574 · see citing works
Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox geneHox-#150;1.6
Chisaka, O., Musci, T. S., & Capecchi, M. R. (1992) · Nature · doi:10.1038/355516a0 · Cited by 536 · see citing works
Neuropathological findings in autism
Palmen, S. J. M. C. (2004) · Brain · doi:10.1093/brain/awh287 · Cited by 527 · see citing works
The intense world syndrome-an alternative hypothesis for autism
Markram, H. (2007) · Frontiers in Neuroscience · doi:10.3389/neuro.01.1.1.006.2007 · Cited by 394 · see citing works
Increased rate of major malformations in offspring exposed to valproate during pregnancy
Wyszynski, D. F., Nambisan, M., Surve, T. Y., Alsdorf, R., Smith, C. R., & Holmes, L. B. (2005) · Neurology · doi:10.1212/01.wnl.0000154516.43630.c5 · Cited by 389 · see citing works
The Contribution of Neuropathologic Studies to the Understanding of Autism
Kemper, T. L., & Bauman, M. L. (1993) · Neurologic Clinics · doi:10.1016/s0733-8619(18)30176-2 · Cited by 373 · see citing works
The Cerebellum and Basal Ganglia are Interconnected
Bostan, A. C., & Strick, P. L. (2010) · Neuropsychology Review · doi:10.1007/s11065-010-9143-9 · Cited by 371 · see citing works
The teratology of autism
Arndt, T. L., Stodgell, C., & Rodier, P. M. (2005) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.11.001 · Cited by 369 · see citing works
Autism-like behaviours with transient histone hyperacetylation in mice treated prenatally with valproic acid
Kataoka, S., Takuma, K., Hara, Y., Maeda, Y., Ago, Y., & Matsuda, T. (2013) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145711001714 · Cited by 341 · see citing works
Fetal Valproate Syndrome: Clinical and Neuro‐developmental Features in Two Sibling Pairs
Christianson, A. L., Chester, N., & Kromberg, J. G. R. (1994) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.1994.tb11858.x · Cited by 340 · see citing works
Gender-specific behavioral and immunological alterations in an animal model of autism induced by prenatal exposure to valproic acid
Schneider, T., Roman, A., Basta‐Kaim, A., Kubera, M., Budziszewska, B., Schneider, K., & Przewłocki, R. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.02.011 · Cited by 335 · see citing works
Autism and Mental Retardation
Williams, R. S. (1980) · Archives of Neurology · doi:10.1001/archneur.1980.00500610029003 · Cited by 318 · see citing works
Cerebellar contributions to the papez circuit
Snider, R. S., & Maiti, A. K. (1976) · Journal of Neuroscience Research · doi:10.1002/jnr.490020204 · Cited by 317 · see citing works
Homozygous HOXA1 mutations disrupt human brainstem, inner ear, cardiovascular and cognitive development
Tischfield, M. A., Bosley, T. M., Salih, M. A. M., Alorainy, I. A., Şener, E. C., Nester, M. J., Oystreck, D. T., Chan, W. M., Andrews, C. V., Erickson, R. P., et al. (2005) · Nature Genetics · doi:10.1038/ng1636 · Cited by 304 · see citing works
Sex differences in autism
Lord, C., Schopler, E., & Revicki, D. (1982) · Journal of Autism and Developmental Disorders · doi:10.1007/bf01538320 · Cited by 303 · see citing works
Fetal Testosterone Influences Sexually Dimorphic Gray Matter in the Human Brain
Lombardo, M. V., Ashwin, E., Auyeung, B., Chakrabarti, B., Taylor, K., Hackett, G., Bullmore, E. T., & Baron-Cohen, S. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4389-11.2012 · Cited by 302 · see citing works
The role of the cerebellum in classical conditioning of discrete behavioral responses
Thompson, R. F., & Steinmetz, J. E. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.01.041 · Cited by 290 · see citing works
The critical period of valproate exposure to induce autistic symptoms in Sprague–Dawley rats
Kim, K. C., Kim, P., Go, H. S., Choi, C. S., Yang, S., Cheong, J. H., Shin, C. Y., & Ko, K. H. (2010) · Toxicology Letters · doi:10.1016/j.toxlet.2010.12.018 · Cited by 285 · see citing works
Abnormality of cerebellar vermian lobules VI and VII in patients with infantile autism: identification of hypoplastic and hyperplastic subgroups with MR imaging.
Courchesne, E., Saitoh, O., Yeung-Courchesne, R., Press, G. A., Lincoln, A. J., Haas, R. H., & Schreibman, L. (1994) · American Journal of Roentgenology · doi:10.2214/ajr.162.1.8273650 · Cited by 278 · see citing works
Cerebellum and Ocular Motor Control
Kheradmand, A., & Zee, D. S. (2011) · Frontiers in Neurology · doi:10.3389/fneur.2011.00053 · Cited by 269 · see citing works
The role of the rhombic lip in avian cerebellum development
Wingate, R. J. T., & Hatten, M. E. (1999) · Development · doi:10.1242/dev.126.20.4395 · Cited by 265 · see citing works
The GABAergic cerebello-olivary projection in the rat
Fredette, B. J., & Mugnaini, E. (1991) · Anatomy and Embryology · doi:10.1007/bf01673258 · Cited by 245 · see citing works
Teratogenicity of sodium valproate
Alsdorf, R., & Wyszynski, D. F. (2005) · Expert Opinion on Drug Safety · doi:10.1517/14740338.4.2.345 · Cited by 237 · see citing works
Topical Review: Fetal Testosterone and Sex Differences in Typical Social Development and in Autism
Knickmeyer, R. C., & Baron-Cohen, S. (2006) · Journal of Child Neurology · doi:10.1177/08830738060210101601 · Cited by 230 · see citing works
Sagittal organization of olivocerebellar and reticulocerebellar projections: Autoradiographic studies with 35S-methionine
Chan‐Palay, V., Palay, S. L., Brown, J. T., & Itallie, C. V. (1977) · Experimental Brain Research · doi:10.1007/bf00237645 · Cited by 214 · see citing works
Male‐specific alteration in excitatory post‐synaptic development and social interaction in pre‐natal valproic acid exposure model of autism spectrum disorder
Kim, K. C., Kim, P., Go, H. S., Choi, C. S., Park, J. H., Kim, H. J., Jeon, S. J., dela Pena, I. C., Han, S., Cheong, J. H., et al. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12147 · Cited by 212 · see citing works
Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning
Gavalas, A., Davenne, M., Lumsden, A., Chambon, P., & Rijli, F. M. (1997) · Development · doi:10.1242/dev.124.19.3693 · Cited by 210 · see citing works
Signalling by FGF8 from the isthmus patterns anterior hindbrain and establishes the anterior limit of Hox gene expression
Irving, C., & Mason, I. J. (2000) · Development · doi:10.1242/dev.127.1.177 · Cited by 197 · see citing works
Valproic Acid Increases Formation of Reactive Oxygen Species and Induces Apoptosis in Postimplantation Embryos: A Role for Oxidative Stress in Valproic Acid-Induced Neural Tube Defects
Tung, E. W. Y., & Winn, L. M. (2011) · Molecular Pharmacology · doi:10.1124/mol.111.072314 · Cited by 196 · see citing works
Roles of Hoxa1 and Hoxa2 in patterning the early hindbrain of the mouse
Barrow, J. R., Stadler, H. S., & Capecchi, M. R. (2000) · Development · doi:10.1242/dev.127.5.933 · Cited by 170 · see citing works
Ectopic Hoxa-1 induces rhombomere transformation in mouse hindbrain
Zhang, M., Kim, H.-J., Marshall, H., et al. (1994) · Development · doi:10.1242/dev.120.9.2431 · Cited by 167 · see citing works
Cerebellar nuclei and the nucleocortical projections in the rat: Retrograde tracing coupled to GABA and glutamate immunohistochemistry
Batini, C., Compoint, C., Buisseret-Delmas, C., et al. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903150106 · Cited by 163 · see citing works
Sex comes in from the cold: the integration of sex and pattern
Christiansen, A. E., Keisman, E. L., Ahmad, S. M., et al. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(02)02769-5 · Cited by 137 · see citing works
Organizational features of the cat and monkey cerebellar nucleocortical projection
Tolbert, D. L., Bantli, H., & Bloedel, J. R. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901820104 · Cited by 127 · see citing works
Neuronal defects in the hindbrain ofHoxa1, Hoxb1andHoxb2mutants reflect regulatory interactions among these Hox genes
Gavalas, A., Ruhrberg, C., Livet, J., Henderson, C. E., & Krumlauf, R. K. (2003) · Development · doi:10.1242/dev.00802 · Cited by 124 · see citing works
Sex-dependent diversity in ventral tegmental dopaminergic neurons and developmental programing: A molecular, cellular and behavioral analysis
Gillies, G. E., Virdee, K., McArthur, S., & Dalley, J. W. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.033 · Cited by 120 · see citing works
Organizational effects of fetal testosterone on human corpus callosum size and asymmetry
Chura, L. R., Lombardo, M. V., Ashwin, E., Bonnie Auyeung, B., Chakrabarti, B., Bullmore, E. T., & Baron‐Cohen, S. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.09.009 · Cited by 119 · see citing works
Autism Attenuates Sex Differences in Brain Structure: A Combined Voxel-Based Morphometry and Diffusion Tensor Imaging Study
Beacher, F. D. C. C., Minati, L., Baron‐Cohen, S., Lombardo, M. V., Lai, M., Gray, M. A., Harrison, N. A., & Critchley, H. (2011) · American Journal of Neuroradiology · doi:10.3174/ajnr.a2880 · Cited by 111 · see citing works
Bacopa monniera (L.) Wettst Ameliorates Behavioral Alterations and Oxidative Markers in Sodium Valproate Induced Autism in Rats
Sandhya, T., Sowjanya, J., & Veeresh, B. (2012) · Neurochemical Research · doi:10.1007/s11064-012-0717-1 · Cited by 103 · see citing works
Mode of Action: Inhibition of Histone Deacetylase, Altering WNT-Dependent Gene Expression, and Regulation of Beta-Catenin—Developmental Effects of Valproic Acid
Wiltse, J. A. (2005) · Critical Reviews in Toxicology · doi:10.1080/10408440591007403 · Cited by 102 · see citing works
Differential regulation of PTEN expression by androgen receptor in prostate and breast cancers
Wang, Y., Romigh, T., He, X., Tan, M.-H., Orloff, M., Silverman, R. H., Heston, W. D. W., & Eng, C. (2011) · Oncogene · doi:10.1038/onc.2011.144 · Cited by 96 · see citing works
The organization of afferents to the cerebellar cortex in the cat: Projections from the deep cerebellar nuclei
Gould, B. B. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901840103 · Cited by 85 · see citing works
Effects of Rat Prenatal Exposure to Valproic Acid on Behaviour and Neuro-Anatomy
Mychasiuk, R., Richards, S., Nakahashi, A., Kolb, B., & Gibb, R. (2012) · Developmental Neuroscience · doi:10.1159/000341786 · Cited by 82 · see citing works
Sex-linked white matter microstructure of the social and analytic brain
Chou, K.-H., Cheng, Y., Chen, I.-Y., Lin, C.-P., & Chu, W.-C. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.07.010 · Cited by 81 · see citing works
Women with autistic-spectrum disorder: magnetic resonance imaging study of brain anatomy
Craig, M., Zaman, S. H., Daly, E., Cutter, W. J., Robertson, D., Hallahan, B. P., Toal, F., Reed, S., Ambikapathy, A., Brammer, M. J., et al. (2007) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.106.034603 · Cited by 79 · see citing works
Increased hippocampal cell density and enhanced spatial memory in the valproic acid rat model of autism
Edalatmanesh, M. A., Nikfarjam, H., Vafaee, F., & Moghadas, M. (2013) · Brain Research · doi:10.1016/j.brainres.2013.06.024 · Cited by 76 · see citing works
Effect of Prenatal Valproic Acid Exposure on Cortical Morphology in Female Mice
Hara, Y., Maeda, Y., Kataoka, S., Ago, Y., Takuma, K., & Matsuda, T. (2012) · Journal of Pharmacological Sciences · doi:10.1254/jphs.12025sc · Cited by 72 · see citing works
The Neuropathology of Autism
Blatt, G. J. (2012) · Scientifica · doi:10.6064/2012/703675 · Cited by 67 · see citing works
Valproic Acid‐Induced Neural Tube Defects
Nau, H. (2007) · Novartis Foundation symposium · doi:10.1002/9780470514559.ch9 · Cited by 66 · see citing works
Integrative classification of morphology and molecular genetics in central nervous system malformations
Sarnat, H. B., & Flores‐Sarnat, L. (2004) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.20663 · Cited by 66 · see citing works
Valproic Acid–Induced Deregulation In Vitro of Genes Associated In Vivo with Neural Tube Defects
Jergil, M., Kultima, K., Gustafson, A.-L., Dencker, L., & Stigson, M. (2009) · Toxicological Sciences · doi:10.1093/toxsci/kfp002 · Cited by 65 · see citing works
Discrimination learning and reversal of the conditioned eyeblink reflex in a rodent model of autism
Stanton, M. E., Peloso, E. D., BROWN, K., & Rodier, P. M. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.10.022 · Cited by 62 · see citing works
Valproic acid-induced changes in gene expression during neurulation in a mouse model
Wlodarczyk, B. J., Craig, J. C., Bennett, G. D., Calvin, J. A., & Finnell, R. H. (1996) · Teratology · doi:10.1002/(sici)1096-9926(199612)54:6 · Cited by 62 · see citing works
Consensus Paper: Current Views on the Role of Cerebellar Interpositus Nucleus in Movement Control and Emotion
Perciavalle, V., Apps, R., Bracha, V., Delgado-Garcia, J. M., Gibson, A. R., Leggio, M. G., Carrel, A. J., Cerminara, N. L., Coco, M., Gruart, A., et al. (2013) · The Cerebellum · doi:10.1007/s12311-013-0464-0 · Cited by 61 · see citing works
GABAergic Cerebellar System In Autism: A Neuropathological And Developmental Perspective
Blatt, G. J. (2005) · International Review of Neurobiology · doi:10.1016/s0074-7742(05)71007-2 · Cited by 56 · see citing works
Functional Significance of Climbing‐Fiber Synchrony
Welsh, J. P. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb07567.x · Cited by 53 · see citing works
Preferential killing of PTEN-null myelomas by PI3K inhibitors through Akt pathway
Zhang, J., Choi, Y., Mavromatis, B. H., et al. (2003) · Oncogene · doi:10.1038/sj.onc.1206718 · Cited by 52 · see citing works
Distribution of Neural Plasticity in Cerebellum-Dependent Motor Learning
Longley, M., & Yeo, C. H. (2014) · Progress in brain research · doi:10.1016/b978-0-444-63356-9.00004-2 · Cited by 49 · see citing works
Cerebellar dentate nuclei lesions reduce motivation in appetitive operant conditioning and open field exploration
Bauer, D. J., Kerr, A. L., & Swain, R. A. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.12.009 · Cited by 48 · see citing works
Induction of the homeotic gene Hoxa1 through valproic acid's teratogenic mechanism of action
Stodgell, C., Ingram, J. L., O’Bara, M. A., Tisdale, B., Nau, H., & Rodier, P. M. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.08.004 · Cited by 47 · see citing works
Effects of cerebellar lesions on activity, social interactions, and other motivated behaviors in the rat.
Berntson, G. G., & Schumacher, K. M. (1980) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077702 · Cited by 44 · see citing works
Sexual dimorphic effect in the genetic association of monoamine oxidase A (MAOA) markers with autism spectrum disorder
Verma, D., Chakraborti, B., Karmakar, A., Bandyopadhyay, T., Singh, A. S., Sinha, S., Chatterjee, A., Ghosh, S., Mohanakumar, K. P., Mukhopadhyay, K., et al. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.11.010 · Cited by 41 · see citing works
The biological basis of autism spectrum disorders: Understanding causation and treatment by clinical geneticists
Geier, D. A., Kern, J. K., & M.R.*, G. (2010) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-2010-1792 · Cited by 36 · see citing works
Integration of multiple motor segments for the elaboration of locomotion: role of the fastigial nucleus of the cerebellum
Mori, S., Nakajima, K., Mori, F., et al. (2004) · Progress in brain research · doi:10.1016/s0079-6123(03)43033-1 · Cited by 34 · see citing works
White Matter Integrity of Specific Dentato-Thalamo-Cortical Pathways is Associated with Learning Gains in Precise Movement Timing
Schulz, R., Wessel, M. J., Zimerman, M., Timmermann, J. E., Gerloff, C. P., & Hummel, F. C. (2014) · Cerebral Cortex · doi:10.1093/cercor/bht356 · Cited by 32 · see citing works
Behavior modification after inactivation of cerebellar dentate nuclei.
Peterson, T. C., Villatoro, L., Arneson, T. J., et al. (2012) · Behavioral Neuroscience · doi:10.1037/a0028701 · Cited by 26 · see citing works
Valproic acid-induced DNA damage increases embryonic p27KIP1 and caspase-3 expression: A mechanism for valproic-acid induced neural tube defects
Tung, E. W. Y., & Winn, L. M. (2011) · Reproductive Toxicology · doi:10.1016/j.reprotox.2011.05.020 · Cited by 25 · see citing works
Is autism due to cerebral–cerebellum disconnection?
Skoyles, J. R. (2002) · Medical Hypotheses · doi:10.1054/mehy.2001.1537 · Cited by 23 · see citing works
Brain morphology in children with 47, XYY syndrome: a voxel‐ and surface‐based morphometric study
Lepage, J., Hong, D. S., Raman, M. M., Marzelli, M., Roeltgen, D. P., Lai, S., ROSS, J. L., & Reiss, A. L. (2013) · Genes Brain & Behavior · doi:10.1111/gbb.12107 · Cited by 21 · see citing works
Interstimulus interval (ISI) discrimination of the conditioned eyeblink response in a rodent model of autism
Murawski, N. J., Brown, K. L., & Stanton, M. E. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.020 · Cited by 20 · see citing works
Nucleus medialis‐nucleus interpositus interface: Its olivary and cerebellocortical projections in the rat
Yatim, N., Buisseret-Delmas, C., Buisseret, P., et al. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903630102 · Cited by 19 · see citing works
The Ontogeny of Associative Cerebellar Learning
Freeman, J. H. (2014) · International review of neurobiology · doi:10.1016/b978-0-12-420247-4.00004-x · Cited by 9 · see citing works
Untitled work
Rodier (1996) · doi:10.1002/(sici)1096-9861(19960624)370:2

Flagged first, then by citations

Sorted by citations

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
Sex differences in autism spectrum disorder: a review
Ferri, S. L., Abel, T., & Brodkin, E. S. (2018) · Current Psychiatry Reports · doi:10.1007/s11920-018-0874-2 · Cited by 392 · see citing works
Sex differences in DNA methylation of the cord blood are related to sex-bias psychiatric diseases
Maschietto, M., Bastos, L. C., Tahira, A. C., Bastos, E. P., Euclydes, V. L. V., Brentani, A., Fink, G., de Baumont, A., Felipe-Silva, A., Francisco, R. P. V., et al. (2017) · Scientific Reports · doi:10.1038/srep44547 · Cited by 78 · see citing works

Authors: Mowery, T. M., Wilson, S. M., Kostylev, P. V., Dina, B., Buchholz, J. B., Prieto, A. L., & Garraghty, P. E.
Affiliations: Indiana University Bloomington (US)
Corresponding author: Mowery, Todd M.
ORCID: Mowery, Todd M.
Wilson, Sarah M.
Kostylev, Polina V.
Dina, Blair
Prieto, Anne L.
Venue: International Journal of Developmental Neuroscience
Publisher: Wiley
Published: 2014-10-31
Volume: 40
Issue: 1
Pages: 15-23
ISSN: 0736-5748 (ISSN-L)
1873-474X
DOI: 10.1016/j.ijdevneu.2014.10.003
OpenAlex: W2049646297
Cited by: 29
References: 90
Citations by year: 2026: 2 · 2024: 2 · 2023: 3 · 2022: 4 · 2021: 1 · 2020: 2 · 2019: 2 · 2018: 4 · 2017: 3 · 2016: 4 · 2015: 2
FWCI: 1.67
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: International Journal of Developmental Neuroscience (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
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Pharmacological Effects and Toxicity Studies
Keywords: valproic acid, autism spectrum disorder, deep cerebellar nuclei, sexual dimorphism, cerebellar morphology, sex differences in brain development, cell number, hindbrain development
MeSH terms: Animals, Animals, Newborn, Cell Count, Cerebellar Nuclei, Child Development Disorders, Pervasive, Disease Models, Animal, Embryo, Mammalian, Enzyme Inhibitors, Female, Male, Sex Characteristics, Valproic Acid, Case-Control Studies, Rats, Long-Evans, Rats

About these checks

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.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Embryological exposure to valproic acid disrupts morphology of the deep cerebellar nuclei in a sexually dimorphic way

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks