CoChat
Sign Up
Cited by 26Genetics and Neurodevelopmental DisordersNeuroscience and Neuropharmacology ResearchAutism Spectrum Disorder Research

Learning and reaction times in mouse touchscreen tests are differentially impacted by mutations in genes encoding postsynaptic interacting proteins SYNGAP1, NLGN3, DLGAP1, DLGAP2 and SHANK2

Open access
Horner, Alexa E., Norris, Rebecca H., McLaren‐Jones, Robbie, Alexander, Liam, Komiyama, Noboru H., Grant, Seth G. N., Nithianantharajah, Jess, Kopanitsa, Maksym V.·2021·Genes, Brain and Behavior
DOI 10.1111/gbb.12723PMC PMC7615670
Open this paper in CoChat — free accountOpen PDF

Abstract

The postsynaptic terminal of vertebrate excitatory synapses contains a highly conserved multiprotein complex that comprises neurotransmitter receptors, cell‐adhesion molecules, scaffold proteins and enzymes, which are essential for brain signalling and plasticity underlying behaviour. Increasingly, mutations in genes that encode postsynaptic proteins belonging to the PSD‐95 protein complex, continue to be identified in neurodevelopmental disorders (NDDs) such as autism spectrum disorder, intellectual disability and epilepsy. These disorders are highly heterogeneous, sharing genetic aetiology and comorbid cognitive and behavioural symptoms. Here, by using genetically engineered mice and innovative touchscreen‐based cognitive testing, we sought to investigate whether loss‐of‐function mutations in genes encoding key interactors of the PSD‐95 protein complex display shared phenotypes in associative learning, updating of learned associations and reaction times. Our genetic dissection of mice with loss‐of‐function mutations in Syngap1, Nlgn3, Dlgap1, Dlgap2 and Shank2 showed that distinct components of the PSD‐95 protein complex differentially regulate learning, cognitive flexibility and reaction times in cognitive processing. These data provide insights for understanding how human mutations in these genes lead to the manifestation of diverse and complex phenotypes in NDDs.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1111/gbb.12723

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

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?

  • PSD95 is a critical postsynaptic protein, involved in the plasticity and stabilization of the synapse.

    “PSD95 is a critical postsynaptic protein, involved in the plasticity and stabilization of the synapse. 37”

    From The MR1/MAIT cell axis enhances dystrophic neurite development in Alzheimer's disease (2025) · cites this paper as [37]

    The Introduction describes PSD-95 as a central organiser of postsynaptic protein complexes involved in synaptic plasticity, supporting its critical postsynaptic role. It says PSD-95 anchors a receptor at the membrane, but does not establish that it stabilizes the synapse itself; that part of the claim is unsupported. No page number is available in our copy. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • In mice lacking various scaffolding or GTPase-activating proteins associated with neurodegenerative disorders, it has been suggested that cognitive performance is worsened with lower PSD95 levels.

    “In line with this idea, in mice lacking various scaffolding or GTPase‐activating proteins that are associated with neurodegenerative disorders, it has been suggested that cognitive performance is worsened with lower PSD95 levels. 37”

    From The MR1/MAIT cell axis enhances dystrophic neurite development in Alzheimer's disease (2025) · cites this paper as [37]

    The Introduction (page unavailable) identifies scaffold proteins and SynGAP as PSD-95 interactors and reports impaired learning in mice completely lacking PSD-95. But it also reports enhanced performance with partial PSD-95 loss; the Discussion (page unavailable) finds normal learning in Dlgap1 mutants and faster learning in Dlgap2 mutants. The paper does not establish that lower PSD-95 levels generally worsen cognition in these mutants, and it associates the genes with neurodevelopmental, not neurodegenerative, disorders. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 72

  1. Bayés A, van de Lagemaat LN, Collins MO, et al. Characterization of the proteome, diseases and evolution of the human postsynaptic den- sity. Nat Neurosci. 2011;14(1):19-21. https://doi.org/10.1038/nn. 2719. · DOI · Paper page
  2. Bayés A, Collins MO, Croning MDR, van de Lagemaat LN, Choudhary JS, Grant SGN. Comparative study of human and mouse postsynaptic proteomes finds high compositional conservation and abundance differences for key synaptic proteins. PLoS One. 2012;7 (10):e46683. https://doi.org/10.1371/journal.pone.0046683. · DOI · Paper page
  3. Distler U, Schmeisser MJ, Pelosi A, et al. In-depth protein profiling of the postsynaptic density from mouse hippocampus using data- independent acquisition proteomics. Proteomics. 2014;14(21-22): 2607-2613. https://doi.org/10.1002/pmic.201300520. · DOI
  4. Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SG. Proteo- mic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci. 2000;3(7):661-669. https://doi.org/10.1038/76615. · DOI · Paper page
  5. Fernández E, Collins MO, Uren RT, et al. Targeted tandem affinity purification of PSD-95 recovers core postsynaptic complexes and schizophrenia susceptibility proteins. Mol Syst Biol. 2009;5:269. https://doi.org/10.1038/msb.2009.27. · DOI
  6. Husi H, Grant SG. Isolation of 2000-kDa complexes of N-methyl-D- aspartate receptor and postsynaptic density 95 from mouse brain. J Neurochem. 2001;77(1):281-291. https://doi.org/10.1046/j.1471- 4159.2001.t01-1-00248.x. · DOI
  7. Frank RAW, Komiyama NH, Ryan TJ, Zhu F, O'Dell TJ. Grant SGN. NMDA receptors are selectively partitioned into complexes and supercomplexes during synapse maturation. Nat Commun. 2016;7: 11264. https://doi.org/10.1038/ncomms11264. · DOI
  8. Frank RAW, Zhu F, Komiyama NH, Grant SGN. Hierarchical organiza- tion and genetically separable subfamilies of PSD95 postsynaptic supercomplexes. J Neurochem. 2017;142(4):504-511. https://doi.org/ 10.1111/jnc.14056. · DOI
  9. Pocklington AJ, Cumiskey M, Armstrong JD, Grant SGN. The proteomes of neurotransmitter receptor complexes form modular networks with distributed functionality underlying plasticity and behaviour. Mol Syst Biol. 2006;2:2006.0023. https://doi.org/10. 1038/msb4100041. · DOI
  10. Coba MP, Pocklington AJ, Collins MO, et al. Neurotransmitters drive combinatorial multistate postsynaptic density networks. Sci Signal. 2009;2(68):ra19. https://doi.org/10.1126/scisignal.2000102. · DOI
  11. Naisbitt S, Kim E, Tu JC, et al. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron. 1999;23(3):569-582.
  12. Chen HJ, Rojas-Soto M, Oguni A, Kennedy MB. A synaptic Ras- GTPase activating protein (p135 SynGAP) inhibited by CaM kinase II. Neuron. 1998;20(5):895-904.
  13. Kim JH, Liao D, Lau LF, Huganir RL. SynGAP: a synaptic RasGAP that associates with the PSD-95/SAP90 protein family. Neuron. 1998;20 (4):683-691.
  14. Kim E, Naisbitt S, Hsueh YP, et al. GKAP, a novel synaptic protein that interacts with the guanylate kinase-like domain of the PSD- 95/SAP90 family of channel clustering molecules. J Cell Biol. 1997; 136(3):669-678. https://doi.org/10.1083/jcb.136.3.669. · DOI · Paper page
  15. Irie M, Hata Y, Takeuchi M, et al. Binding of neuroligins to PSD-95. Sci- ence. 1997;277(5331):1511-1515. https://doi.org/10.1126/science. 277.5331.1511. · DOI · Paper page
  16. Kopanitsa MV, Lagemaat LN v d, Afinowi NO, et al. A combinatorial postsynaptic molecular mechanism converts patterns of nerve impulses into the behavioral repertoire. bioRxiv. 2018;500447. https://doi.org/10.1101/500447. · DOI
  17. Komiyama NH, Lagemaat LN v d, Stanford LE, et al. Synaptic combi- natorial molecular mechanisms generate repertoires of innate and learned behavior. bioRxiv. 2018;500389. https://doi.org/10.1101/ 500389. · DOI
  18. Luo J, Tan JM, Nithianantharajah J. A molecular insight into the disso- ciable regulation of associative learning and motivation by the synap- tic protein neuroligin-1. BMC Biol. 2020;18(1):118. https://doi.org/ 10.1186/s12915-020-00848-7. · DOI
  19. Verma V, Paul A, Amrapali Vishwanath A, Vaidya B, Clement JP. Understanding intellectual disability and autism spectrum disorders from common mouse models: synapses to behaviour. Open Biol. 2019;9(6):180265. https://doi.org/10.1098/rsob.180265. · DOI
  20. Hamdan FF, Gauthier J, Spiegelman D, et al. Mutations in SYNGAP1 in autosomal nonsyndromic mental retardation. N Engl J Med. 2009; 360(6):599-605. https://doi.org/10.1056/NEJMoa0805392. · DOI · Paper page
  21. Mignot C, von Stulpnagel C, Nava C, et al. Genetic and neu- rodevelopmental spectrum of SYNGAP1-associated intellectual dis- ability and epilepsy. J Med Genet. 2016;53(8):511-522. https://doi. org/10.1136/jmedgenet-2015-103451. · DOI
  22. Berryer MH, Hamdan FF, Klitten LL, et al. Mutations in SYNGAP1 cause intellectual disability, autism, and a specific form of epilepsy by inducing haploinsufficiency. Hum Mutat. 2013;34(2):385-394. https://doi.org/10.1002/humu.22248. · DOI · Paper page
  23. Jamain S, Quach H, Betancur C, et al. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat Genet. 2003;34(1):27-29. https://doi.org/10.1038/ng1136. · DOI · Paper page
  24. Stewart SE, Yu D, Scharf JM, et al. Genome-wide association study of obsessive-compulsive disorder. Mol Psychiatry. 2013;18(7):788-798. https://doi.org/10.1038/mp.2012.85. · DOI · Paper page
  25. Peykov S, Berkel S, Schoen M, et al. Identification and functional characterization of rare SHANK2 variants in schizophrenia. Mol Psychiatry. 2015;20(12):1489-1498. https://doi.org/10.1038/mp. 2014.172. · DOI
  26. Quartier A, Courraud J, Thi Ha T, et al. Novel mutations in NLGN3 causing autism spectrum disorder and cognitive impairment. Hum Mutat. 2019;40(11):2021-2032. https://doi.org/10.1002/humu. 23836. · DOI
  27. Parenti I, Rabaneda LG, Schoen H, Novarino G. Neu- rodevelopmental disorders: from genetics to functional pathways. Trends Neurosci. 2020;43(8):608-621. https://doi.org/10.1016/j.tins. 2020.05.004. · DOI
  28. Sahin M, Sur M. Genes, circuits, and precision therapies for autism and related neurodevelopmental disorders. Science. 2015;350(6263): aab3897. https://doi.org/10.1126/science.aab3897. · DOI · Paper page
  29. Canitano R. Epilepsy in autism spectrum disorders. Eur Child Adolesc Psychiatry. 2007;16(1):61-66. https://doi.org/10.1007/s00787-006- 0563-2. · DOI
  30. Keller R, Basta R, Salerno L, Elia M. Autism, epilepsy, and synaptopathies: a not rare association. Neurol Sci. 2017;38(8):1353- 1361. https://doi.org/10.1007/s10072-017-2974-x. · DOI
  31. Luo J, Norris RH, Gordon SL, Nithianantharajah J. Neu- rodevelopmental synaptopathies: insights from behaviour in rodent models of synapse gene mutations. Prog Neuropsychopharmacol Biol Psychiatry. 2018;84(Pt B):424-439. https://doi.org/10.1016/j.pnpbp. 2017.12.001. · DOI
  32. Horner AE, Heath CJ, Hvoslef-Eide M, et al. The touchscreen operant platform for testing learning and memory in rats and mice. Nat Protoc. 2013;8(10):1961-1984. https://doi.org/10.1038/nprot.2013.122. · DOI
  33. Bussey TJ, Holmes A, Lyon L, et al. New translational assays for pre- clinical modelling of cognition in schizophrenia: the touchscreen test- ing method for mice and rats. Neuropharmacology. 2012;62(3):1191- 1203. https://doi.org/10.1016/j.neuropharm.2011.04.011. · DOI · Paper page
  34. Ryan TJ, Kopanitsa MV, Indersmitten T, et al. Evolution of GluN2A/B cytoplasmic domains diversified vertebrate synaptic plasticity and behavior. Nat Neurosci. 2013;16(1):25-32. https://doi.org/10.1038/ nn.3277. · DOI
  35. Nithianantharajah J, McKechanie AG, Stewart TJ, et al. Bridging the translational divide: identical cognitive touchscreen testing in mice and humans carrying mutations in a disease-relevant homologous gene. Sci Rep. 2015;5:14613. https://doi.org/10.1038/srep14613. · DOI
  36. Norris RHC, Churilov L, Hannan AJ, Nithianantharajah J. Mutations in neuroligin-3 in male mice impact behavioral flexibility but not rela- tional memory in a touchscreen test of visual transitive inference. Mol Autism. 2019;10:42. https://doi.org/10.1186/s13229-019-0292-2. · DOI
  37. Horner AE, McLaughlin CL, Afinowi NO, et al. Enhanced cognition and dysregulated hippocampal synaptic physiology in mice with a het- erozygous deletion of PSD-95. Eur J Neurosci. 2018;47(2):164-176. https://doi.org/10.1111/ejn.13792. · DOI
  38. Brigman JL, Feyder M, Saksida LM, Bussey TJ, Mishina M, Holmes A. Impaired discrimination learning in mice lacking the NMDA receptor NR2A subunit. Learn Mem. 2008;15(2):50-54. https://doi.org/10. 1101/lm.777308. · DOI
  39. Brigman JL, Daut RA, Saksida L, Bussey TJ, Nakazawa K, Holmes A. Impaired discrimination learning in interneuronal NMDAR-GluN2B mutant mice. Neuroreport. 2015;26(9):489-494. https://doi.org/10. 1097/WNR.0000000000000373. · DOI
  40. Komiyama NH, Watabe AM, Carlisle HJ, et al. SynGAP regulates ERK/MAPK signaling, synaptic plasticity, and learning in the complex with postsynaptic density 95 and NMDA receptor. J Neurosci. 2002; 22(22):9721-9732.
  41. Varoqueaux F, Aramuni G, Rawson RL, et al. Neuroligins determine synapse maturation and function. Neuron. 2006;51(6):741-754. https://doi.org/10.1016/j.neuron.2006.09.003. · DOI
  42. Piiponniemi TO, Bragge T, Vauhkonen EE, et al. Acquisition and reversal of visual discrimination learning in APPSwDI/Nos2(-/-) (CVN) mice. Neurosci Lett. 2017;650:126-133. https://doi.org/10. 1016/j.neulet.2017.04.049. · DOI
  43. Heckers S, Zalesak M, Weiss AP, Ditman T, Titone D. Hippocampal activation during transitive inference in humans. Hippocampus. 2004; 14(2):153-162. https://doi.org/10.1002/hipo.10189. · DOI
  44. Muhia M, Yee BK, Feldon J, Markopoulos F, Knuesel I. Disruption of hippocampus-regulated behavioural and cognitive processes by het- erozygous constitutive deletion of SynGAP. Eur J Neurosci. 2010;31 (3):529-543. https://doi.org/10.1111/j.1460-9568.2010.07079.x. · DOI · Paper page
  45. Guo X, Hamilton PJ, Reish NJ, Sweatt JD, Miller CA, Rumbaugh G. Reduced expression of the NMDA receptor-interacting protein SynGAP causes behavioral abnormalities that model symptoms of schizophrenia. Neuropsychopharmacology. 2009;34(7):1659-1672. https://doi.org/10.1038/npp.2008.223. · DOI · Paper page
  46. Muhia M, Feldon J, Knuesel I, Yee BK. Appetitively motivated instrumental learning in SynGAP heterozygous knockout mice. Behav Neurosci. 2009;123(5):1114-1128. https://doi.org/10.1037/ a0017118. · DOI
  47. Radyushkin K, Hammerschmidt K, Boretius S, et al. Neuroligin- 3-deficient mice: model of a monogenic heritable form of autism with an olfactory deficit. Genes Brain Behav. 2009;8(4):416-425. https:// doi.org/10.1111/j.1601-183X.2009.00487.x. · DOI
  48. Coba MP, Ramaker MJ, Ho EV, et al. Dlgap1 knockout mice exhibit alterations of the postsynaptic density and selective reductions in sociability. Sci Rep. 2018;8(1):2281. https://doi.org/10.1038/s41598- 018-20610-y. · DOI
  49. Jiang-Xie L-F, Liao H-M, Chen C-H, et al. Autism-associated gene Dlgap2 mutant mice demonstrate exacerbated aggressive behaviors and orbitofrontal cortex deficits. Mol Autism. 2014;5(1):32. https:// doi.org/10.1186/2040-2392-5-32. · DOI
  50. Rasmussen AH, Rasmussen HB, Silahtaroglu A. The DLGAP family: neuronal expression, function and role in brain disorders. Mol Brain. 2017;10(1):43. https://doi.org/10.1186/s13041-017-0324-9. · DOI · Paper page
  51. Schmeisser MJ, Ey E, Wegener S, et al. Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2. Nature. 2012;486 (7402):256-260. https://doi.org/10.1038/nature11015. · DOI · Paper page
  52. Pappas AL, Bey AL, Wang X, et al. Deficiency of Shank2 causes mania-like behavior that responds to mood stabilizers. JCI Insight. 2017;2(20):e92052. https://doi.org/10.1172/jci.insight.92052. · DOI
  53. Ey E, Torquet N, de Chaumont F, et al. Shank2 mutant mice dis- play hyperactivity insensitive to methylphenidate and reduced flexibility in social motivation, but normal social recognition. Front Mol Neurosci. 2018;11:365. https://doi.org/10.3389/fnmol.2018. 00365. · DOI
  54. Graybeal C, Bachu M, Mozhui K, et al. Strains and stressors: an analy- sis of touchscreen learning in genetically diverse mouse strains. PLoS One. 2014;9(2):e87745. https://doi.org/10.1371/journal.pone. 0087745. · DOI
  55. Laughlin RE, Grant TL, Williams RW, Jentsch JD. Genetic dis- section of behavioral flexibility: reversal learning in mice. Biol Psychi- atry. 2011;69(11):1109-1116. https://doi.org/10.1016/j.biopsych. 2011.01.014. · DOI
  56. Nolan SO, Reynolds CD, Smith GD, et al. Deletion of Fmr1 results in sex-specific changes in behavior. Brain Behav. 2017;7(10):e00800. https://doi.org/10.1002/brb3.800. · DOI
  57. Arbogast T, Razaz P, Ellegood J, et al. Kctd13-deficient mice display short-term memory impairment and sex-dependent genetic interac- tions. Hum Mol Genet. 2019;28(9):1474-1486. https://doi.org/10. 1093/hmg/ddy436. · DOI · Paper page
  58. Zamarbide M, Mossa A, Muñoz-Llancao P, et al. Male-specific cAMP signaling in the hippocampus controls spatial memory deficits in a mouse model of autism and intellectual disability. Biol Psychiatry. 2019;85(9):760-768. https://doi.org/10.1016/j.biopsych.2018. 12.013. · DOI
  59. Saré RM, Lemons A, Figueroa C, Song A, Levine M, Beebe Smith C. Sex-selective effects on behavior in a mouse model of tuberous scle- rosis complex. eNeuro. 2020;7(2):ENEURO.0379-ENEU19.2020. https://doi.org/10.1523/ENEURO.0379-19.2020. · DOI
  60. Fertan E, Wong AA, Purdon MK, Weaver ICG, Brown RE. The effect of background strain on the behavioral phenotypes of the MDGA2 +/-mouse model of autism spectrum disorder. Genes Brain Behav. 2020;18:e12696. https://doi.org/10.1111/gbb.12696. · DOI
  61. Jaramillo TC, Escamilla CO, Liu S, Peca L, Birnbaum SG, Powell CM. Genetic background effects in Neuroligin-3 mutant mice: minimal behavioral abnormalities on C57 background. Autism Res. 2018;11(2): 234-244. https://doi.org/10.1002/aur.1857. · DOI
  62. Turner KM, Simpson CG, Burne THJ. BALB/c mice can learn touchscreen visual discrimination and reversal tasks faster than C57BL/6 mice. Front Behav Neurosci. 2017;11:16. https://doi.org/10. 3389/fnbeh.2017.00016. · DOI
  63. Kumar G, Talpos J, Steckler T. Strain-dependent effects on acquisition and reversal of visual and spatial tasks in a rat touchscreen battery of cognition. Physiol Behav. 2015;144:26-36. https://doi.org/10.1016/j. physbeh.2015.03.001. · DOI · Paper page
  64. Wong AA, Brown RE. Age-related changes in visual acuity, learning and memory in C57BL/6J and DBA/2J mice. Neurobiol Aging. 2007; 28(10):1577-1593. https://doi.org/10.1016/j.neurobiolaging.2006. 07.023. · DOI
  65. Kuo SS, Wojtalik JA, Mesholam-Gately RI, Keshavan MS, Eack SM. Transdiagnostic validity of the MATRICS consensus cognitive battery across the autism-schizophrenia spectrum. Psychol Med. 2020;50(10): 1623-1632. https://doi.org/10.1017/S0033291719001582. · DOI
  66. Ewen JB, Shapiro BK. Disorders of attention or learning in neu- rodevelopmental disorders. Semin Pediatr Neurol. 2005;12(4):229- 241. https://doi.org/10.1016/j.spen.2005.12.005. · DOI
  67. Chmielewski WX, Beste C. Action control processes in autism spec- trum disorder-insights from a neurobiological and neuroanatomical perspective. Prog Neurobiol. 2015;124:49-83. https://doi.org/10. 1016/j.pneurobio.2014.11.002. · DOI
  68. De Rubeis S, Buxbaum JD. Genetics and genomics of autism spec- trum disorder: embracing complexity. Hum Mol Genet. 2015;24(R1): R24-31. https://doi.org/10.1093/hmg/ddv273. · DOI · Paper page
  69. Zhu F, Cizeron M, Qiu Z, et al. Architecture of the mouse brain syn- aptome. Neuron. 2018;99(4):781-799.e10. https://doi.org/10.1016/j. neuron.2018.07.007. · DOI
  70. Cizeron M, Qiu Z, Koniaris B, et al. A brainwide atlas of synapses across the mouse life span. Science. 2020;369(6501):270-275. https://doi.org/10.1126/science.aba3163. · DOI
  71. Nithianantharajah J, Grant SGN. Cognitive components in mice and humans: combining genetics and touchscreens for medical translation. Neurobiol Learn Mem. 2013;105:13-19. https://doi.org/10.1016/j. nlm.2013.06.006. · DOI
  72. Beraldo FH, Palmer D, Memar S, et al. MouseBytes, an open-access high-throughput pipeline and database for rodent touchscreen-based cognitive assessment. Elife. 2019;8:e49630. https://doi.org/10.7554/ eLife.49630. · DOI

Cited by

Sorted by citations

Authors
Horner, A. E., Norris, R. H., McLaren‐Jones, R., Alexander, L., Komiyama, N. H., Grant, S. G. N., Nithianantharajah, J., & Kopanitsa, M. V.
Affiliations
  • Synome (United Kingdom) (GB)
  • The University of Melbourne (AU)
  • Synome Ltd, Babraham Research Campus Cambridge UK
  • Simons Initiative for the Developing Brain (GB)
  • UK Dementia Research Institute (GB)
Corresponding author
  • Nithianantharajah, Jess
  • Kopanitsa, Maksym V.
ORCID
Venue
Genes, Brain and Behavior
Publisher
Wiley
Published
2020-12-29
Volume
20
Issue
1
Pages
e12723-e12723
ISSN
  • 1601-183X (ISSN-L)
  • 1601-1848
DOI
10.1111/gbb.12723
PMC
PMC7615670
OpenAlex
W3117999865
Cited by
26
References
6
Citations by year
2026: 4 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 9 · 2021: 4 · 2020: 1
FWCI
2.45
Type
journal article
Language
en
Open access
Licence
Locations
  • Genes Brain & Behavior (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion, cc-by)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
  • UCL Discovery (University College London) (submittedVersion)
  • Minerva Access (University of Melbourne) (submittedVersion, cc-by)
Funders
  • Australian Research Council (Future Fellowship 140101327)
  • H2020 European Research Council (695568 SYNNOVATE)
  • Medical Research Council Canada (UK Dementia Research Institute at Imperial College)
  • National Health and Medical Research Council (1083334, 1163504)
  • Seventh Framework Programme (grant agreement No 604102 (Human Brain project))
  • Simons Foundation Autism Research Initiative (529085)
  • Wellcome Trust (Technology Development Grant 202932)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Keywords
postsynaptic proteins, SYNGAP1, neuroligin-3, DLGAP1, Shank2, loss-of-function mutations, neurodevelopmental disorders, autism spectrum disorder, intellectual disability, epilepsy, associative learning, cognitive flexibility, reaction time, genetically modified mice
MeSH terms
Loss of Function Mutation, SAP90-PSD95 Associated Proteins, Animals, Female, Learning, Male, Membrane Proteins, Mice, Inbred C57BL, Nerve Tissue Proteins, Reaction Time, Cell Adhesion Molecules, Neuronal, ras GTPase-Activating Proteins, Mice

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