Repetitive behavior and increased activity in mice with Purkinje cell loss: a model for understanding the role of cerebellar pathology in autism
Open accessAbstract
Repetitive behaviors and hyperactivity are common features of developmental disorders, including autism. Neuropathology of the cerebellum is also a frequent occurrence in autism and other developmental disorders. Recent studies have indicated that cerebellar pathology may play a causal role in the generation of repetitive and hyperactive behaviors. In this study, we examined the relationship between cerebellar pathology and these behaviors in a mouse model of Purkinje cell loss. Specifically, we made aggregation chimeras between Lc/+ mutant embryos and +/+ embryos. Lc/+ mice lose 100% of their Purkinje cells postnatally due to a cell‐intrinsic gain‐of‐function mutation. Through our histological examination, we demonstrated that Lc/+↔+/+ chimeric mice have Purkinje cells ranging from zero to normal numbers. Our analysis of these chimeric cerebella confirmed previous studies on Purkinje cell lineage. The results of both open‐field activity and hole‐board exploration testing indicated negative relationships between Purkinje cell number and measures of activity and investigatory nose‐poking. Additionally, in a progressive‐ratio operant paradigm, we found that Lc/+ mice lever‐pressed significantly less than +/+ controls, which led to significantly lower breakpoints in this group. In contrast, chimeric mice lever‐pressed significantly more than controls and this repetitive lever‐pressing behavior was significantly and negatively correlated with total Purkinje cell numbers. Although the performance of Lc/+ mice is probably related to their motor deficits, the significant relationships between Purkinje cell number and repetitive lever‐pressing behavior as well as open‐field activity measures provide support for a role of cerebellar pathology in generating repetitive behavior and increased activity in chimeric mice.
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There was a negative relationship between Purkinje cell number and investigatory nose poking in a hole-board exploration task.
“(3) investigatory nose poking in a hole-board exploration task [287].”
From Consensus Paper: Pathological Role of the Cerebellum in Autism (2012) · cites this paper as [287]
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Cites
Statistical principles in experimental design.
Winer, B. J. (1962) · McGraw-Hill Book Company · doi:10.1037/11774-000 · Cited by 27,137 · see citing works
Statistical Principles in Experimental Design
Myers, J. L., & Winer, B. J. (1964) · The American Journal of Psychology · doi:10.2307/1419292 · Cited by 8,111 · see citing works
Dementia Praecox or the Group of Schizophrenias
(1951) · Journal of the American Medical Association · doi:10.1001/jama.1951.02920270079043 · Cited by 4,407 · see citing works
Estimation of nuclear population from microtome sections
Abercrombie, M. (1946) · The Anatomical Record · doi:10.1002/ar.1090940210 · Cited by 4,363 · see citing works
Simonoff, E., Pickles, A., Charman, T., Chandler, S., Loucas, T., & Baird, G. (2008) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b013e318179964f · Cited by 3,399 · see citing works
Varieties of Repetitive Behavior in Autism: Comparisons to Mental Retardation
Bodfish, J. W., Symons, F. J., Parker, D. E., & Lewis, M. H. (2000) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1005596502855 · Cited by 1,223 · see citing works
Progressive Ratio as a Measure of Reward Strength
Hodos, W. (1961) · Science · doi:10.1126/science.134.3483.943 · Cited by 1,147 · see citing works
Neurodegeneration in Lurcher mice caused by mutation in δ2 glutamate receptor gene
Zuo, J., De Jager, P. L., Takahashi, K. A., Jiang, W., Linden, D. J., & Heintz, N. (1997) · Nature · doi:10.1038/42009 · Cited by 554 · 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
Structural and quantitative studies on the normal C3H and lurcher mutant mouse
Caddy, K. W. T., & Biscoe, T. J. (1979) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1979.0055 · Cited by 484 · see citing works
Evidence for a cerebellar role in reduced exploration and stereotyped behavior in autism
Pierce, K., & Courchesne, E. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01008-8 · Cited by 464 · see citing works
The estrous cycle affects cocaine self-administration on a progressive ratio schedule in rats
Roberts, D. C. S., Bennett, S. A. L., & Vickers, G. J. (1989) · Psychopharmacology · doi:10.1007/bf00451696 · Cited by 372 · see citing works
EFFECTS OF INCREMENT SIZE AND REINFORCER VOLUME ON PROGRESSIVE RATIO PERFORMANCE
Hodos, W., & Kalman, G. (1963) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1963.6-387 · Cited by 302 · see citing works
The psychology of perseverative and stereotyped behaviour
Ridley, R. M. (1994) · Progress in Neurobiology · doi:10.1016/0301-0082(94)90039-6 · Cited by 287 · see citing works
Roberts, D. C. S., Loh, E. A., & Vickers, G. (1989) · Psychopharmacology · doi:10.1007/bf00439560 · Cited by 243 · see citing works
Repetitive behaviors in autistic disorder.
Militerni, R., Bravaccio, C., Falco, C., Fico, C., & Palermo, M. T. (2002) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-002-0279-x · Cited by 235 · see citing works
Stereotypies and hyperactivity in rhesus monkeys exposed to IgG from mothers of children with autism
Martin, L. A., Ashwood, P., Braunschweig, D., Cabanlit, M., Van de Water, J., & Amaral, D. G. (2008) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.12.007 · Cited by 231 · see citing works
Self-citationWetts, R., & Herrup, K. (1982) · Brain Research · doi:10.1016/0006-8993(82)90431-0 · Cited by 222 · see citing works
Maternal neuronal antibodies associated with autism and a language disorder
Dalton, P., Deacon, R., Blamire, A., Pike, M., McKinlay, I., Stein, J., Styles, P., & Vincent, A. (2003) · Annals of Neurology · doi:10.1002/ana.10557 · Cited by 204 · cited 2× · see citing works
“…of ASD is self-generated or maternally derived pathogenic antibodies and several recent studies have shown that antibodies from children with ASD or their mothers target cell populations within the cerebellum including Purkinje cells (Dalton et al., 2003; Singer et al., 2006; Wills et al., 2009).”
BackgroundWetts, R., & Herrup, K. (1982) · Development · doi:10.1242/dev.68.1.87 · Cited by 198 · see citing works
Kennedy, C. H., Meyer, K. A., Knowles, T., & Shukla, S. (2000) · Journal of Applied Behavior Analysis · doi:10.1901/jaba.2000.33-559 · Cited by 180 · see citing works
Wills, S., Cabanlit, M., Bennett, J., Ashwood, P., Amaral, D. G., & Van de Water, J. (2009) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2008.07.007 · Cited by 163 · see citing works
Mullen, R. J., & Whitten, W. K. (1971) · Journal of Experimental Zoology · doi:10.1002/jez.1401780203 · Cited by 159 · see citing works
Effects of environmental complexity on stereotyped behaviours of children
Hutt, C., & Hutt, S. J. (1965) · Animal Behaviour · doi:10.1016/0003-3472(65)90064-3 · Cited by 154 · see citing works
Antibrain antibodies in children with autism and their unaffected siblings
Singer, H. S., Morris, C. M., Williams, P. N., Yoon, D. Y., Hong, J. J., & Zimmerman, A. W. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2006.05.025 · Cited by 132 · see citing works
Retrospective clonal analysis of the cerebellum using genetic laacZ/lacZ mouse mosaics
Mathis, L., Bonnerot, C., Puelles, L., & Nicolas, J.-F. (1997) · Development · doi:10.1242/dev.124.20.4089 · Cited by 114 · see citing works
Mittleman, G., Goldowitz, D., Heck, D. H., & Blaha, C. D. (2008) · Synapse · doi:10.1002/syn.20525 · Cited by 111 · see citing works
Self-citationJentsch, D. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00174-3 · Cited by 104 · see citing works
Techniques for the Genetic Analysis of Brain and Behavior: Focus on the Mouse
Goldowitz, D., Wahłsten, D., & Wimer, R. E. (1992) · Medical Entomology and Zoology · Cited by 103 · see citing works
Self-citationRole of the cerebellum in exploration behavior
Caston, J., Chianale, C., Delhaye‐Bouchaud, N., & Mariani, J. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00847-6 · Cited by 89 · see citing works
Skjoldager, P. D., Pierre, P. J., & Mittleman, G. (1993) · Learning and Motivation · doi:10.1006/lmot.1993.1019 · Cited by 88 · see citing works
Self-citationThe hippocampus and reward: Effects of hippocampal lesions on progressive-ratio responding.
Schmelzeis, M. C., & Mittleman, G. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.5.1049 · Cited by 81 · see citing works
Self-citationSchwabe, K., Klein, S., & Koch, M. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.11.005 · Cited by 55 · see citing works
Martin, L. A., Goldowitz, D., & Mittleman, G. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02921.x · Cited by 55 · see citing works
Self-citationWinger, G. D., & Woods, J. H. (1985) · Drug and Alcohol Dependence · doi:10.1016/0376-8716(85)90036-5 · Cited by 50 · see citing works
Baader, S. L., Schilling, M. L., Rosengarten, B., Pretsch, W., Teutsch, H. F., Oberdick, J., & Schilling, K. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0083 · Cited by 49 · see citing works
Pattern formation in the cerebellum of murine embryonic stem cell chimeras
Hawkes, R., Faulkner-Jones, B. E., Tam, P., & Tan, S. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00085.x · Cited by 39 · see citing works
A special type of head stereotypies in children with developmental (?cerebellar) disorder:
Hottinger-Blanc, P. M., Ziegler, A., & Deonna, T. W. (2002) · European Journal of Paediatric Neurology · doi:10.1053/ejpn.2002.0582 · Cited by 36 · see citing works
Martin, L. A., Escher, T., Goldowitz, D., & Mittleman, G. (2004) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2004.00067.x · Cited by 36 · see citing works
Self-citationBoltshauser, E., Steinlin, M. I., Martin, E., & Deonna, T. (1996) · Neuropediatrics · doi:10.1055/s-2007-973748 · Cited by 31 · see citing works
Hole poking and motor coordination in lurcher mutant mice
Lalonde, R., Joyal, C. C., Guastavino, J.-M., & Botez, M. I. (1993) · Physiology & Behavior · doi:10.1016/0031-9384(93)90041-d · Cited by 28 · see citing works
Soliva, J. C., Carmona, S., Fauquet, J., Hoekzema, E. A., Bulbena, A., Hilferty, J., & Vilarroya, Ó. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04604.x · Cited by 25 · see citing works
Exploration of a hole-board matrix in nervous mutant mice
Lalonde, R., & Botez, M. I. (1985) · Brain Research · doi:10.1016/0006-8993(85)90755-3 · Cited by 20 · see citing works
Sustained attention in the mouse: A study of the relationship with the cerebellum.
Martin, L. A., Goldowitz, D., & Mittleman, G. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.2.477 · Cited by 17 · see citing works
Self-citationBuprenorphine, heroin, and methadone: Comparison of relative reinforcing properties.
Mello, N. K., Bree, M. P., & Mendelson, J. H. (1984) · PsycEXTRA Dataset · doi:10.1037/e468882004-001 · Cited by 9 · see citing works
The role of the cortical parts of the cerebellar hemispheres in discrimination learning of cats
Davis, H. N., Watkins, G. M., Angermeier, W. F., & Rubia, F. J. (1970) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00586974 · Cited by 7 · see citing works
Flagged first, then by citations
1 of the 47 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Consensus Paper: Pathological Role of the Cerebellum in Autism
Fatemi, S. H., Aldinger, K. A., Ashwood, P., Bauman, M. L., Blaha, C. D., Blatt, G. J., Chauhan, A., Chauhan, V., Dager, S. R., Dickson, P. E., et al. (2012) · The Cerebellum · doi:10.1007/s12311-012-0355-9 · Cited by 723 · see citing works
Self-citationWöhr, M., Orduz, D., Gregory, P., Moreno, H., Khan, U., Vörckel, K. J., Wolfer, D. P., Welzl, H., Gall, D., Schiffmann, S. N., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.19 · Cited by 258 · see citing works
Autism spectrum disorders and neuropathology of the cerebellum
Hampson, D. R., & Blatt, G. J. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00420 · Cited by 247 · see citing works
Reith, R. M., McKenna, J., Wu, H. C., Hashmi, S. S., Cho, S., Dash, P. K., & Gambello, M. J. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.10.014 · Cited by 191 · see citing works
Steadman, P. E., Ellegood, J., Szulc, K. U., Turnbull, D. H., Joyner, A. L., Henkelman, R. M., & Lerch, J. P. (2013) · Autism Research · doi:10.1002/aur.1344 · Cited by 169 · see citing works
Wöhr, M., & Scattoni, M. L. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.047 · Cited by 178 · see citing works
Autistic-Like Traits and Cerebellar Dysfunction in Purkinje Cell PTEN Knock-Out Mice
Cupolillo, D., Hoxha, E., Faralli, A., Luca, A. D., Rossi, F., Tempia, F., & Carulli, D. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.339 · Cited by 162 · see citing works
Roles of mTOR Signaling in Brain Development
Lee, D. Y. (2015) · Experimental Neurobiology · doi:10.5607/en.2015.24.3.177 · Cited by 162 · see citing works
Altered Peripheral and Central Inflammatory Responses in a Mouse Model of Autism
Lucchina, L., & Depino, A. M. (2013) · Autism Research · doi:10.1002/aur.1338 · Cited by 142 · see citing works
Is autism a disease of the cerebellum? An integration of clinical and pre-clinical research
Rogers, T. D., McKimm, E. J., Dickson, P., Goldowitz, D., Blaha, C., & Mittleman, G. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00015 · Cited by 141 · see citing works
Self-citationAutoantibodies to cerebellum in children with autism associate with behavior
Goines, P., Haapanen, L., Boyce, R., Duncanson, P., Braunschweig, D., Delwiche, L., Hansen, R., Hertz-Picciotto, I., Ashwood, P., & Van de Water, J. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.11.017 · Cited by 134 · see citing works
Rogers, T. D., Dickson, P. E., Heck, D. H., Goldowitz, D., Mittleman, G., & Blaha, C. D. (2011) · Synapse · doi:10.1002/syn.20960 · Cited by 120 · see citing works
Self-citationMonoamine 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
Ravizza, S. M., Solomon, M., Ivry, R. B., & Carter, C. S. (2013) · Development and Psychopathology · doi:10.1017/s0954579413000163 · Cited by 94 · see citing works
Eissa, N., Sadeq, A. S., Sasse, A., & Sadek, B. S. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00886 · Cited by 97 · see citing works
Rogers, T. D., Dickson, P. E., McKimm, E., Heck, D. H., Goldowitz, D., Blaha, C. D., & Mittleman, G. (2013) · The Cerebellum · doi:10.1007/s12311-013-0462-2 · Cited by 89 · see citing works
Self-citationFrom mice to men: lessons from mutant ataxic mice
Cendelín, J. (2014) · Cerebellum & Ataxias · doi:10.1186/2053-8871-1-4 · Cited by 83 · 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
Ady, V., Perroy, J., Tricoire, L., Piochon, C., Dadak, S., Chen, X., Dusart, I., Fagni, L., Lambolez, B., & Levenes, C. (2014) · The EMBO Reports · doi:10.1002/embr.201337371 · Cited by 75 · see citing works
The cerebellum and neuropsychiatric disorders
Villanueva, R. (2012) · Psychiatry Research · doi:10.1016/j.psychres.2012.02.023 · Cited by 73 · see citing works
AKAPs integrate genetic findings for autism spectrum disorders
Poelmans, G., Franke, B., Pauls, D. L., Glennon, J. C., & Buitelaar, J. K. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.48 · Cited by 72 · see citing works
Vazquez-Sanroman, D. B., Sanchis‐Segura, C., Toledo‐Cárdenas, M. R., Hernández‐Aguilar, M. E., Manzo, J. G., & Miquel, M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.12.047 · Cited by 63 · see citing works
The dopaminergic system dynamic in the time perception: a review of the evidence
Marinho, V., de Oliveira, A. T., Rocha, K. D. M., Ribeiro, J. A., Magalhães, F. E. X., Bento, T., Pinto, G. R., Velasques, B., Ribeiro, P. F. M., Silva, L. W. D. G., et al. (2017) · International Journal of Neuroscience · doi:10.1080/00207454.2017.1385614 · Cited by 60 · see citing works
Antipsychotic pharmacogenomics in first episode psychosis: a role for glutamate genes
Stevenson, J. M., Reilly, J. L., Harris, M. S. H., Patel, S., Weiden, P. J., Prasad, K. M. R., Badner, J. A., Nimgaonkar, V. L., Keshavan, M. S., Sweeney, J. A., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.10 · Cited by 60 · see citing works
Behavioral flexibility in a mouse model of developmental cerebellar Purkinje cell loss
Dickson, P. E., Rogers, T. D., Mar, N. D., Martin, L. A., Heck, D., Blaha, C. D., Goldowitz, D., & Mittleman, G. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.05.010 · Cited by 59 · see citing works
Self-citationPathways to Drug Development for Autism Spectrum Disorders
Hampson, D. R., Gholizadeh, S., & Pacey, L. K. K. (2011) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.2011.245 · Cited by 55 · see citing works
Macrı̀, S., Biamonte, F., Romano, E., Marino, R., Keller, F., & Laviola, G. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.03.012 · Cited by 55 · see citing works
Dean, S. L., Wright, C. L., Hoffman, J. F., Wang, M., Alger, B. E., & McCarthy, M. M. (2012) · Endocrinology · doi:10.1210/en.2012-1350 · Cited by 51 · see citing works
Pacey, L. K. K., Doss, L., Cifelli, C., van der Kooy, D., Heximer, S. P., & Hampson, D. R. (2011) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.12.005 · Cited by 46 · see citing works
Hegarty, J. P., Weber, D. J., Cirstea, C. M., & Beversdorf, D. Q. (2018) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-018-3613-y · Cited by 46 · see citing works
Eissa, N., Azimullah, S., Jayaprakash, P., Jayaraj, R. L., Reiner‐Link, D., Ojha, S. K., Beiram, R., Stark, H., Łażewska, D., Kieć‐Kononowicz, K., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113996 · Cited by 45 · see citing works
Martin, L. A., Sample, H. A., Gregg, M., & Wood, C. A. (2014) · Brain and Behavior · doi:10.1002/brb3.273 · Cited by 43 · see citing works
Self-citationZhang, L., Chung, S. K., & Chow, B. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.344 · Cited by 41 · see citing works
Clinical and Neurobiological Relevance of Current Animal Models of Autism Spectrum Disorders
Kim, K. C., Gonzales, E. L., Lázaro, M. T., Choi, C. S., Bahn, G. H., Yoo, H. J., & Shin, C. Y. (2016) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2016.061 · Cited by 40 · see citing works
Mechanisms of Compartmental Purkinje Cell Death and Survival in the Lurcher Mutant Mouse
Armstrong, C. L., Duffin, C. A., McFarland, R. J., & Vogel, M. W. (2010) · The Cerebellum · doi:10.1007/s12311-010-0231-4 · Cited by 35 · see citing works
Cerebellar contribution to higher and lower order rule learning and cognitive flexibility in mice
Dickson, P. E., Cairns, J., Goldowitz, D., & Mittleman, G. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.03.040 · Cited by 32 · see citing works
Self-citationNeurocognitive and cerebellar function in ADHD, autism and spinocerebellar ataxia
Cundari, M., Vestberg, S., Gustafsson, P., Gorcenco, S., & Rasmussen, A. (2023) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2023.1168666 · Cited by 34 · see citing works
Learning by observation in children with autism spectrum disorder
Foti, F., Mazzone, L., Menghini, D., Peppo, L. D., Federico, F., Postorino, V., Baumgartner, E., Valeri, G., Petrosini, L., & Vicari, S. (2014) · Psychological Medicine · doi:10.1017/s003329171300322x · Cited by 30 · see citing works
Thomas, S. D., Abdalla, S., Eissa, N., Akour, A., Jha, N., Ojha, S., & Sadek, B. (2024) · Pharmaceuticals · doi:10.3390/ph17070831 · Cited by 24 · see citing works
Poleg, S., Kourieh, E., Ruban, A., Shapira, G., Shomron, N., Barak, B., & Offen, D. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01612-3 · Cited by 26 · see citing works
Kawa, R., & E.*, P. (2010) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-2010-1785 · Cited by 25 · see citing works
Elgamal, M. A., Khodeer, D. M., Abdel‐Wahab, B. A., Ibrahim, I. A. A., Alzahrani, A. R., Moustafa, Y. M., Ali, A. A., & El-Sayed, N. M. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1113966 · Cited by 20 · see citing works
Seyedinia, S. A., Tarahomi, P., Abbarin, D., Sedaghat, K., Rashidy‐Pour, A., Yaribeygi, H., Vafaei, A. A., & Raise‐Abdullahi, P. (2023) · Metabolic Brain Disease · doi:10.1007/s11011-023-01275-7 · Cited by 19 · see citing works
Examining the genetic and neural components of cognitive flexibility using mice
Brigman, J. L., Powell, E. M., Mittleman, G., & Young, J. W. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.12.024 · Cited by 19 · see citing works
Self-citationMejı́as, R., Chiu, S., Han, M., Rose, R., Gil-Infante, A., Zhao, Y., Huganir, R. L., & Wang, T. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104602 · Cited by 18 · see citing works
The Role of MicroRNAs in Cerebellar Development and Autism Spectrum Disorder During Embryogenesis
Constantin, L. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0220-9 · Cited by 17 · see citing works
McKimm, E., Corkill, B., Goldowitz, D., Albritton, L. M., Homayouni, R., Blaha, C. D., & Mittleman, G. (2013) · The Cerebellum · doi:10.1007/s12311-013-0541-4 · Cited by 16 · see citing works
Self-citationAutism Spectrum Disorder: The Cerebellum, Genes, and Pathways
D’Mello, S. R. (2025) · Neurology International · doi:10.3390/neurolint17100173 · Cited by 14 · see citing works
Rauf, S., Soesatyo, M. H. N. E., Agustiningsih, D., & Partadiredja, G. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112481 · Cited by 12 · see citing works
Weisner, P. A., Chen, C., Sun, Y., Yoo, J., Kao, W., Zhang, H., Baltz, E. T., Troy, J. M., & Stubbs, L. J. (2019) · G3 Genes Genomes Genetics · doi:10.1534/g3.119.400723 · Cited by 12 · see citing works
Social impairments in mice lacking the voltage-gated potassium channel Kv3.1
Bee, S., Ringland, A., & Coutellier, L. D. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113468 · Cited by 11 · see citing works
Social Deficits and Cerebellar Degeneration in Purkinje Cell Scn8a Knockout Mice
Yang, X., Yin, H., Wang, X., Sun, Y., Bian, X., Zhang, G., Li, A., Cao, A., Li, B., Ebrahimi‐Fakhari, D., et al. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.822129 · Cited by 11 · see citing works
Abnormal grooming activity in Dab1 (scrambler) mutant mice
Strazielle, C., Lefèvre, A., Jacquelin, C., & Lalonde, R. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.038 · Cited by 11 · see citing works
Kútna, V., O’Leary, V. B., Höschl, C., & Ovsepian, S. V. (2022) · Autism Research · doi:10.1002/aur.2688 · Cited by 10 · see citing works
Mohamed, A. F., El-Gammal, M. A., El-Yamany, M. F., & Khodir, A. E. (2024) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2024.111192 · Cited by 8 · see citing works
Chen, Z., Long, H., Guo, J., Wang, Y., He, K., Tao, C., Li, X., Jiang, K., Guo, S., & ., Y. P. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.901682 · Cited by 8 · see citing works
Hormones and Cerebellar Development
Koibuchi, N., & Ikeda, Y. (2012) · Springer eBooks · doi:10.1007/978-94-007-1333-8_16 · Cited by 8 · see citing works
Zhou, P., Peng, S., Wen, S., Lan, Q., Zhuang, Y., Li, X., Shi, M., & Zhang, C. (2024) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s485487 · Cited by 7 · see citing works
The Hole-Board Test in Mutant Mice
Lalonde, R., & Strazielle, C. (2022) · Behavior Genetics · doi:10.1007/s10519-022-10102-1 · Cited by 7 · see citing works
Abbarin, D., Vafaei, A. A., Rashidy‐Pour, A., Bandegi, A. R., Taherian, A., Rahmani, M., Jarrahi, M., & Sedaghat, K. (2023) · Middle East Journal of Rehabilitation and Health Studies · doi:10.5812/mejrh-129627 · Cited by 7 · see citing works
Meng, L. M., Lü, L., Murphy, K. M., Yuede, C. M., Cheverud, J. M., Csernansky, J. G., & Dong, H. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.05.017 · Cited by 7 · see citing works
Autism Spectrum Disorders and Ataxia
Fatemi, S. H., & Folsom, T. D. (2012) · Springer eBooks · doi:10.1007/978-94-007-1333-8_87 · Cited by 7 · see citing works
Mittleman, G., & Blaha, C. D. (2015) · Contemporary clinical neuroscience · doi:10.1007/978-1-4939-2190-4_11 · Cited by 5 · see citing works
Self-citationInfluence of the Cerebellum in Anticipation and Mental Disorders
Hilber, P. (2016) · Springer eBooks · doi:10.1007/978-3-319-45142-8_8 · Cited by 4 · see citing works
Abbott, P. W., Hardie, J. B., Walsh, K. P., Nessler, A. J., Farley, S. J., Freeman, J. H., Wemmie, J. A., Wendt, L. H., Kim, Y.-C., Sowers, L. P., et al. (2024) · The Cerebellum · doi:10.1007/s12311-023-01648-9 · Cited by 4 · see citing works
The Purkinje Cell: As an Integrative Machine
Vilmint, A. G., Dorgans, K., Roux, S., & Bossu, J. L. (2016) · Springer eBooks · doi:10.1007/978-3-319-24551-5_21 · Cited by 4 · see citing works
Cerebellar purkinje cell dysfunction contributes to gait impairments in Shank3-mutant mice
Liu, H., Huang, X., Ma, G., Zhao, X., Xia, R., Li, Z., Guo, B., Wu, S., & Wang, W. (2026) · Molecular Autism · doi:10.1186/s13229-026-00704-5 · Cited by 2 · see citing works
King, C., Maze, T., & Plakke, B. (2024) · Experimental Brain Research · doi:10.1007/s00221-024-06902-y · Cited by 2 · see citing works
Environmental Enrichment: A New Therapy Based on Findings in Animal Models of Autism
Rahimian, S., Yazdi, A. A., & Edalatmanesh, M. A. (2016) · The Neuroscience Journal of Shefaye Khatam · doi:10.18869/acadpub.shefa.4.4.89 · Cited by 2 · see citing works
Gaytán-Tocavén, L., López‐Vázquez, M. A., Guevara, M. Á., & Olvera‐Cortés, M. E. (2017) · Experimental Brain Research · doi:10.1007/s00221-017-5014-4 · Cited by 2 · see citing works
Loss of Purkinje cells in the developing cerebellum strengthens the cerebellothalamic synapsesPreprint
Nishiyama, H., Nishiyama, N., & Zemelman, B. V. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.01.564864 · Cited by 2 · see citing works
Shariatmadari, H., Bigdeli, M. R., Khaksar, S., & Vahidi, S. (2026) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000889 · Cited by 1 · see citing works
L1-79 and the Role of Catecholamines in Autism
Rothman, J. (2021) · IntechOpen eBooks · doi:10.5772/intechopen.95052 · Cited by 1 · see citing works
Autism Spectrum Disorders and Ataxia
Folsom, T. D., & Fatemi, S. H. (2021) · Springer eBooks · doi:10.1007/978-3-030-23810-0_87 · Cited by 1 · see citing works
The role of CADM1 in energy and glucose homeostasis
Matthäus, D. (2014) · doi:10.18452/16905 · Cited by 1 · see citing works
CHARACTERIZATION AND TREATMENT OF A NOVEL MOUSE MODEL OF TSC-ASSOCIATED AUTISM
Reith, R. M. (2012) · Digital Commons-TMC (Texas Medical Center)
Modeling SHANK2 Related Neuropsychiatric Disorders in Mice
Pappas, A. L. (2015) · DukeSpace (Duke University)
Hormones and Cerebellar Development
Koibuchi, N., & Ikeda, Y. (2021) · Springer eBooks · doi:10.1007/978-3-030-23810-0_16
Hormones and Cerebellar Development
Koibuchi, N., & Ikeda, Y. (2020) · Springer eBooks · doi:10.1007/978-3-319-97911-3_16-2
Autism Spectrum Disorders and Ataxia
Folsom, T. D., & Fatemi, S. H. (2020) · Springer eBooks · doi:10.1007/978-3-319-97911-3_87-2
- Authors
- Martin, L. A., Goldowitz, D., & Mittleman, G.
- Affiliations
- Azusa Pacific University (US)
- University of Tennessee Health Science Center (US)
- University of Memphis (US)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2010-02
- Volume
- 31
- Issue
- 3
- Pages
- 544-555
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- PMC
- PMC2846709
- OpenAlex
- W2035069442
- Cited by
- 82
- References
- 47
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 5 · 2023: 5 · 2022: 4 · 2021: 5 · 2020: 5 · 2019: 2 · 2018: 2 · 2017: 2 · 2016: 7 · 2015: 7 · 2014: 4 · 2013: 11 · 2012: 11
- FWCI
- 6.00
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01NS063009)
- 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 › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- Purkinje cell degeneration, cerebellar pathology, autism spectrum disorder, repetitive behavior, hyperactivity, open field behavior, nose-poking, motor impairment
- MeSH terms
- Animals, Autistic Disorder, Behavior, Animal, Cerebellum, Child, Chimera, Female, Humans, Male, Mice, Neurologic Mutants, Motor Activity, Neuropsychological Tests, Pregnancy, Purkinje Cells, Mice
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