The neuron-specific chromatin regulatory subunit BAF53b is necessary for synaptic plasticity and memory.
- Authors
- Vogel-Ciernia, Annie; Matheos, Dina P; Barrett, Ruth M; Kramár, Enikö A; Azzawi, Soraya; Chen, Yuncai; Magnan, Christophe N; Zeller, Michael; Sylvain, Angelina; Haettig, Jakob; Jia, Yousheng; Tran, Anthony; Dang, Richard; Post, Rebecca J; Chabrier, Meredith; Babayan, Alex H; Wu, Jiang I; Crabtree, Gerald R; Baldi, Pierre; Baram, Tallie Z; Lynch, Gary; Wood, Marcelo A
- Year
- 2013
- Journal
- Nature neuroscience
- PMID
- 23525042
- DOI
- 10.1038/nn.3359
- PMCID
- PMC3777648
Recent exome sequencing studies have implicated polymorphic Brg1-associated factor (BAF) complexes (mammalian SWI/SNF chromatin remodeling complexes) in several human intellectual disabilities and cognitive disorders. However, it is currently unknown how mutations in BAF complexes result in impaired cognitive function. Postmitotic neurons express a neuron-specific assembly, nBAF, characterized by the neuron-specific subunit BAF53b. Mice harboring selective genetic manipulations of BAF53b have severe defects in long-term memory and long-lasting forms of hippocampal synaptic plasticity. We rescued memory impairments in BAF53b mutant mice by reintroducing BAF53b in the adult hippocampus, which suggests a role for BAF53b beyond neuronal development. The defects in BAF53b mutant mice appeared to derive from alterations in gene expression that produce abnormal postsynaptic components, such as spine structure and function, and ultimately lead to deficits in synaptic plasticity. Our results provide new insight into the role of dominant mutations in subunits of BAF complexes in human intellectual and cognitive disorders.
Characterization of BAF53bΔHD and Baf53b+/− het mice. (a) Wildtype BAF53b is diagramed with hydrophobic domain (HD) shown in grey. In the BAF53bΔHD construct the amino acids 323-333 within the hydrophobic domain were deleted. The BAF53bΔHD mutant sequence was cloned into a separate vector containing intron and exon sequences with splice sites and the SV40 intron and polyadenylation signal, which was then cloned downstream of the 8.5 kb mouse CaMKIIα promoter. This construct was used to generate BAF53bΔHD transgenic mice. (b) Quantitative RT-PCR was performed with transgene specific primers to measure transgene expression in dorsal hippocampus of two independently derived lines of BAF53bΔHD mice. We identified two significantly different lines (Mann-Whitney U (18)=0.00, p<0.0001): a low expressing line (n=10) and a high expressing line (n=10) (2 out of 12 founder lines). (c) Wildtype BAF53b expression in the dorsal hippocampus of BAF53bΔHDhigh (n=10) and BAF53bΔHDlow (n=11) is not significantly different (Kruskal-Wallis H2,33=4.03, p=0.13) between mutant mice and wildtype littermates (n=15). (d) Quantitative RT-PCR shows that wildtype Baf53b expression in the dorsal hippocampus of Baf53b+/− het mice (n=13) is significantly (2-way ANOVA main effect of genotype F1,18=17.87, p<0.001) reduced compared to wildtype littermates (n=8). There was no effect of behavior (F1,18=0.81, p=0.38) or interaction (F1,18=0.40, p=0.53) Mean (± SEM). (e) Western blot analysis shows that BAF53b protein in dorsal hippocampus of Baf53b+/− het mice (n=13) is significantly (2-way ANOVA main effect of genotype F1,17=345.0, p<0.0001) reduced compared to wildtype littermates (n=9). There was no effect of behavior (F1,17=0.05, p=0.82) or interaction (F1,17=0.03, p=0.85).
BAF53bΔHD and Baf53b+/− het mice have impaired long-term memory. (a) Mice received 10 min training in an environment with 2 identical objects and received a retention test 24 hrs later in which one object is moved to a new location (OLM). (b) BAF53bΔHDhigh mutant mice (n=9) and BAF53bΔHDlow (n=13) exhibit a significant 24 hr long-term OLM deficit (ANOVA F2,34=5.79, p<0.01) in a hippocampus-dependent task as compared to wildtype littermates (n=15) and were not significantly different from zero (BAF53bΔHDhigh t-test t(8)=0.39, p=0.71 and BAF53bΔHDlow t-test t(12)=0.19, p=0.85). There were no significant differences in total exploration time between the groups during testing (ANOVA F2,34=0.45, p=0.64) or training (ANOVA F2,34=1.13, p=0.33) (c) Baf53b+/− het mice (n=16) exhibit impaired long-term OLM compared to wildtype mice (n=6; t-test t(20)=2.35, p<0.05). There was no difference in overall exploration between the groups at training t-test t(20)=0.40, p=0.70 or testing t-test t(20)=0.95, p=0.35. (d) Mice received 10 min training in an environment with 2 identical objects and received a retention test 24 hrs later in which one object is replaced with a novel one. (e) In a hippocampus-independent object recognition task, BAF53bΔHDhigh mutant mice (n=12) and BAF53bΔHDlow (n=11) exhibit significant ORM deficits as compared to wildtype mice (n=18; Kruskal-Wallis H2,38=10.72, p<0.01; t(11)=13.06, p<0.05 and t(10)=11.43, p<0.05, respectively, Dunn's post hoc tests). There were no differences in total exploration time between the groups at training Kruskal-Wallis H2,38=0.61, p=0.98 or testing ANOVA F(2,30)=2.53, p=0.09. (f) Baf53b+/− het mice (n=9) exhibit impaired long-term OLM compared to wildtype mice (n=10; t-test t(17)=2.88, p<0.05). There was no difference in the overall exploration time between the groups at training t-test t(17)=0.60, p=0.56 or testing t-test t(17)=0.36, p=0.72. Mean (± SEM).
BAF53bΔHDlow and Baf53b+/− het mice have impairments in long-term memory for contextual fear, but normal cued fear memory. (a) During contextual fear training velocity (cm s−1) did not differ between BAF53bΔHDlow (n=10) and wildtype (n=9) mice for the five second prior to shock (Pre-Shock) nor during the shock (Shock) (Repeated Measures ANOVA F1,17=234.2, p<0.0001, bonferroni post hoc t-test pre-shock vs. post shock for wildtypes t-test t(8)=10.09, p<0.001 and BAF53bΔHDlow t-test t(9)=11.60, p<0.001, and no effect of genotype ANOVA F1,17=0.44, p=0.51 or interaction F1,17=0.44, p=0.51). (b) Animals were tested in the conditioned context 24 hours after conditioning. BAF53bΔHDlow mutant mice froze significantly less then wildtypes (t-test t(17)=3.46, p<0.05). At test there was a significant main effect of sex (ANOVA F1,15=12.39, p=0.003) but no interaction with genotype (F1,15=0.03, p=0.86) with males freezing more then females for BAF53bΔHDlow (bonferroni post hoc t-test t(9)=2.58, p<0.05) and a similar (but not significant) trend in wildtypes (bonferroni post hoc t-test t(8)=2.40, p>0.05). (c) 24hr memory test for cued fear conditioning (test in novel context). Both groups exhibited similar levels of freezing prior to tone onset (Pre-Tone) and after Tone onset (Tone) (Repeated Measures ANOVA F1,16=0.98, p=0.77), with a significant increase in freezing following tone onset in both groups (F1,16=38.21, p<0.0001, bonferroni post hoc t-test Pre-Tone vs. Tone for wildtype (n=8) t(7)=3.21, p<0.05 and BAF53bΔHDlow (n=10) t(9)=5.68, p<0.001). (D) Baf53b+/− het mice (n=9) have a normal response to the shock during contextual fear training compared to wildtype littermates (n=8) with a significant increase in velocity following shock for both groups (Repeated Measures ANOVA F1,15=183.3, p<0.0001), bonferroni post hoc t-test pre-shock vs. post shock for wildtype t(7)=8.38, p<0.001 and Baf53b+/− het mice t(8)=10.85, p<0.001, and no effect of genotype (F1,15=2.57, p=0.13) or interaction F1,15=1.80, p=0.20). (E) Baf53b+/− het mice froze significantly less then wildtypes at the 24hr long-term contextual fear memory test (t-test t(15)=2.25, p<0.05) (F) 24hr memory test for cued fear conditioning (test in novel context). Both groups exhibited similar levels of freezing prior to tone onset (Pre-Tone) and after Tone onset (Tone) (Repeated Measures ANOVA F1,22=0.53, p=0.48) with a significant increase in freezing following tone onset in both groups (ANOVA F1,22=63.29, p<0.0001, bonferroni post hoc t-test Pre-Tone vs. Tone for wildtype (n=12) t(11)=6.56, p<0.001 and Baf53b+/− het mice (n=12) t(11)=4.69, p<0.001). Mean (± SEM).
Hippocampal AAV-Baf53b rescues OLM but not ORM deficits in Baf53b+/− het mice. (a) Representative images of immunofluorescence of BAF53b (yellow) expression in wildtype and Baf53b+/− het mice with control (AAV-hrGFP) or AAV-Baf53b. Nuclei (blue) were counterstained with DAPI. Scale bar 200μm. (b) Mean intensity of BAF53b immunofluorescence from CA1 cell layer normalized to background (corpus collosum) and wildtype AAV-hrGFP. There is a complete return of BAF53b expression in CA1 of Baf53b+/− het mice to wildtype levels (ANOVA no main effect genotype F1,38=2.23, p=0.14, a main effect of virus F1,38=8.14, p<0.01, and a significant interaction F1,38=5.34, p<0.05). Bonferroni post hoc t-test WT vs. Baf53b+/− het mice for AAV-hrGFP t-test t(16)=2.5, p<0.05 and AAV-Baf53b t-test t(22)=0.62, p>0.05. WT AAV-hrGFP (n=10), WT AAV-Baf53b (n=12), Baf53b+/− het mice AAV-hrGFP (n=9), Baf53b+/− het mice AAV-Baf53b (n=12). (C) Schematic of behavioral testing. OLM was conducted as described in the methods. Following a five day rest period, animals then were habituated to a novel context and then underwent ORM training and testing. (D) Long-term Object Location Memory (OLM) (24hrs). There is a complete rescue of OLM in Baf53b+/− het mice with AAV-Baf53b (2-way ANOVA main effect genotype F1,40=4.49, p<0.05, virus F1,40=6.04, p<0.05, and no interaction F1,40=1.76 p=0.19). Bonferroni post hoc t-test WT vs. Baf53b+/− het mice for AAV-hrGFP t-test t(18)=2.33, p<0.05 and AAV-Baf53b t-test t(22)=0.59, p>0.05. There was no difference between any of the groups for total exploration at training (2-way ANOVA no effect genotype F1,40=3.56, p=0.07, virus F1,40=0.02, p=0.90, and no interaction F1,40=0.63 p=0.43) or testing (2-way ANOVA no effect genotype F1,40=0.29, p=0.59, virus F1,40=0.53, p=0.47, and no interaction F1,40=4.02 p=0.05). WT AAV-hrGFP (n=10), WT AAV-Baf53b (n=12), Baf53b+/− het mice AAV-hrGFP (n=10), Baf53b+/− het mice AAV-Baf53b (n=12). (E) Long-term Object Recognition Memory (ORM) (24hrs). There is a no rescue of ORM in Baf53b+/− het mice with AAV-Baf53b expression in dorsal hippocampus (2-way ANOVA main effect genotype F1,33=12.79, p<0.01, no main effect of virus F1,33=0.08 p=0.77, and no interaction F1, 33=0.16, p=0.69). Bonferroni post hoc t-test WT vs. Baf53b+/− het mice for AAV-hrGFP t-test t(14)=2.63, p<0.05 and AAV-Baf53b t-test t(19)=2.42, p<0.05). There was no difference between any of the groups for total exploration at training (2-way ANOVA no effect genotype F1,33=1.08, p=0.31, virus F1,33=2.85, p=0.10, and no interaction F1,33=0.04 p=0.84) or testing (2-way ANOVA no effect genotype F1,33=4.13, p=0.05, virus F1,33=1.78, p=0.19, and no interaction F1,33=0.51 p=0.48). WT AAV-hrGFP (n=7), WT AAV-Baf53b (n=10), Baf53b+/− het mice AAV-hrGFP (n=9), Baf53b+/− het mice AAV-Baf53b (n=11). Mean (± SEM).
BAF53bΔHD and Baf53b+/− het mice have disrupted LTP in hippocampal slices. (A, B) Simultaneous recordings of fEPSP slope from slices receiving baseline stimulation (control, grey circle) and 10 theta bursts (TBS) for wildtype (WT) (open circle) and Baf53b+/− het slices (green circle). Baf53b+/− het slices fail to maintain stable LTP (average for last 5min) t-test t(26)=6.48, p<0.0001. BAF53bΔHDlow slices produced stable potentiation similar to wildtype slices t(8)=0.30, p=0.79. (C) LTP induced with 5 theta bursts delivered to one of the two stimulation electrodes (control, grey circles) produced stable potentiation in wildtype slices (open circles) but not in BAF53bΔHDlow slices (green circles) t(13)=3.77, p<0.01. (D) Simultaneous recordings of fEPSP slope in slices receiving low-frequency stimulation (grey circles) and 10 theta bursts (open and green circles) in wildtype and BAF53bΔHDhigh slices t(22)=3.49, p<0.01. (E) Input/Output curves measuring the magnitude of the fEPSP response across a range of stimulation currents (10-50 μA) was comparable between Baf53b+/− het, BAF53bΔHDlow and wildtype slices, but not BAF53bΔHDhigh mice. (2-way Repeated ANOVA main effect genotype F3,35=4.47, p<0.01, time F8,35=246.7, p<0.0001, and significant interaction F24,35=2.01 p<0.005). For each stimulation current bonferroni post hoc t-test for wildtype (n=20) vs. Baf53b+/− het slices (n=6), wildtype (n=20) vs. BAF53bΔHDhigh slices (n=7), and wildtype (n=20) vs. BAF53bΔHDlow slices (n=6) are given in Supplemental FigS4. (**p<0.01; *p<0.05). (F) Input/Output curves compare amplitudes of the presynaptic fiber volley to the fEPSP amplitude across a range of stimulation currents. Left, Input/output curves were not different between Baf53b+/− het mice (n=6), BAF53bΔHDlow (n=6), and wildtype (n=6) (ANOVA F2,15=1.04, p=0.38). Right, The slope was significantly reduced in the Input/Output curve produced from BAF53bΔHDhigh slices (n=12) relative to wildtype (n=12) bathed in aCSF containing 3mM Mg+ and 1mM Ca2+ (Mann-Whitney U(22)=3.00, p<0.0001). (G) Paired pulse facilitation of the initial slope of the synaptic response was comparable (40, 60, 100, and 200 ms inter-pulse intervals) in slices from Baf53b+/− het (n=9), BAF53bΔHDlow (n=7), and wildtype mice (n=14) but not in BAF53bΔHDhigh slices (n=6) (2-way Repeated ANOVA main effect genotype F3,32=11.60, p<0.0001, interval F3,32=192.6, p<0.0001, and significant interaction F9,32=3.31 p<0.005). Bonnferoni post hoc comparisons in Supplemental FigS4 (***p<0.001; ** p<0.01; *p<0.05). (H) Top; sample traces of mini excitatory postsynaptic currents (mEPSCs) recorded from BAF53bΔHDhigh (n=14) and wildtype (n=15) neurons. Bottom; There were no differences in mEPSCs from BAF53bΔHDhigh and wildtype for the amplitude (left, t(27)=0.75, p=0.46) and frequency (right, t(27)=0.52, p=0.61) of the events in slices.
TBS induced phosphorylation (p) of Cofilin is altered in Baf53b+/− het mice. Adult mouse hippocampal slices are stimulated electrophysiologically and immunolabeled. (A) Immunocytochemical labeling of pCofilin (left) and PSD95-immunoreactive puncta (green) display some co-localization (Scale 2.5um). (B) Distribution of double labeled pCofilin intensities, show that Baf53b+/− het mice have a different baseline distribution, with an increase in the more intensely labeled puncta. (C) Cumulative probability distributions show that the Baf53b+/− het mice have curves that are shifted to the right relative to their wildtype counterparts, thus favoring the more intense puncta. (D) Bar graph shows values of double labeled puncta 7 minutes after control stimulation or TBS, with values normalized to respective control stimulation group. ANOVA main effect of stimulation F1,25=14.92, p<0.005, genotype F1,25=5.13, p<0.05, and a significant interaction F1,25=5.11, p<0.05. Bonnferoni corrected post hoc t-test wildtype control vs. TBS t(12)=4.24, p<0.001; Baf53b+/− het control vs. TBS t(13)=1.16, p>0.05 wildtype control (n=8), wildtype TBS (n=8), Baf53b+/− het control (n=7), Baf53b+/− het TBS (n=8). Mean +/- SEM. (E) Left Quantification of the mean volumes of PSD95-immuno reactive puncta that were colocalized with pCofilin for Baf53b+/− het mice (n=15) and wildtype littermates (n=16) t-test t(29)=1.39, p=0.19. Right Mean intensities of PSD95 labeled elements also show no difference between the Baf53b+/− het mice (n=15) and wildtype littermates (n=16) t-test t(29)=1.47, p=0.15. “n” refers to the number of images analyzed with ∼40,000 PSD95 immunoreactive puncta per image.
Differential gene expression in Baf53b+/− het mice by RNA Sequencing. (A) Gene expression diagram for wildtype compared to Baf53b+/− het mice mutant mice sacrificed directly from the homecage. (B) Gene expression for genes that increased or decreased expression following behavior (sacrificed 30min post training) compared to homecage. Genes with differential expression at homecage were removed prior to analysis. “Both” indicates genes regulated similarly in wildtype and Baf53b+/− het mice. “Unique Increase” comprises genes that increase in only the indicated genotype. “Unique Decrease” comprises genes that decrease in only the indicated genotype. Groups: Baf53b+/− het mice homecage (Baf53b+/− HC) (n=6); Baf53b+/− het mice Behavior (Baf53b+/− Beh) (n=6); wildtype homecage (WT HC) (n=6); and wildtype behavior (WT Beh) (n=6). Total gene counts for each genotype given above or below each column. (C) qRTP-PCR validation of the IEG c-fos. ANOVA main effect of behavior F1,20=157.6, p<0.0001, no effect of genotype F1,20=0.49, p=0.49, and no interaction F1,20=0.45, p=0.51. Expression relative to gapdh and normalized to wildtype homecage. (D) qRTP-PCR validation of the IEG Egr2. ANOVA main effect of behavior F1,20=224.2, p<0.0001, no effect of genotype F1,20=1.53, p=0.23, and no interaction F1,20=0.55, p=0.47. Expression relative to gapdh and normalized to wildtype homecage.
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| Uncoupling memory impairments from autism-associated behaviors in Chd2 deficient mice. | Yoon SH et al. | — | 2026 | → |
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| Developmental and Epileptic Encephalopathy: Pathogenesis of Intellectual Disability Beyond Channelopathies. | Medyanik AD et al. | — | 2025 | → |
| Genetic Mechanisms of Experience-Dependent Neuronal Plasticity. | West AE | — | 2025 | → |
| HDAC3 as an Emerging Therapeutic Target for Alzheimer's Disease and other Neurological Disorders. | Li Y et al. | — | 2025 | → |
| Hippocampal transcriptome profiling associated with post-traumatic stress disorder-like behaviors in male mice. | He Z et al. | — | 2025 | → |
| Role of Hypothalamic CRH Neurons in Regulating the Impact of Stress on Memory and Sleep. | Wiest A et al. | — | 2025 | → |
| Structural plasticity of pyramidal cell neurons measured after FLASH and conventional dose-rate irradiation. | Dickstein DL et al. | — | 2025 | → |
| Activity-assembled nBAF complex mediates rapid immediate early gene transcription by regulating RNA polymerase II productive elongation. | Cornejo KG et al. | — | 2024 | → |
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| A Survey on AI-Driven Mouse Behavior Analysis Applications and Solutions. | Guo C et al. | — | 2024 | → |
| BRG1 establishes the neuroectodermal chromatin landscape to restrict dorsal cell fates. | Hoffman JA et al. | — | 2024 | → |
| Epigenetic Regulation and Neurodevelopmental Disorders: From MeCP2 to the TCF20/PHF14 Complex. | Dominguez G et al. | — | 2024 | → |
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| Small molecule modulators of chromatin remodeling: from neurodevelopment to neurodegeneration. | Jiang D et al. | — | 2023 | → |
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| The BAF chromatin remodeling complexes: structure, function, and synthetic lethalities. | Varga J et al. | — | 2021 | → |
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| A neuroscientist's guide to transgenic mice and other genetic tools. | Navabpour S et al. | — | 2020 | → |
| ATP-Dependent Chromatin Remodeling Complex in the Lineage Specification of Mesenchymal Stem Cells. | Du W et al. | — | 2020 | → |
| Bcl11 Transcription Factors Regulate Cortical Development and Function. | Simon R et al. | — | 2020 | → |
| Conditional Dnmt3b deletion in hippocampal dCA1 impairs recognition memory. | Kong Q et al. | — | 2020 | → |
| <i>In Vivo</i> Attenuation of M-Current Suppression Impairs Consolidation of Object Recognition Memory. | Kosenko A et al. | — | 2020 | → |
| Investigating Memory Updating in Mice Using the Objects in Updated Locations Task. | Wright DS et al. | — | 2020 | → |
| Loss of the neural-specific BAF subunit ACTL6B relieves repression of early response genes and causes recessive autism. | Wenderski W et al. | — | 2020 | → |
| Mammalian SWI/SNF Chromatin Remodeling Complexes in Embryonic Stem Cells: Regulating the Balance Between Pluripotency and Differentiation. | Ye Y et al. | — | 2020 | → |
| Neural substrates of habit. | Malvaez M | — | 2020 | → |
| Optogenetic intervention of seizures improves spatial memory in a mouse model of chronic temporal lobe epilepsy. | Kim HK et al. | — | 2020 | → |
| Persistence of Fear Memory Depends on a Delayed Elevation of BAF53b and FGF1 Expression in the Lateral Amygdala. | Yoo M et al. | — | 2020 | → |
| Resolving the Synaptic versus Developmental Dichotomy of Autism Risk Genes. | Heavner WE et al. | — | 2020 | → |
| Rho Guanine Nucleotide Exchange Factor 4 (Arhgef4) Deficiency Enhances Spatial and Object Recognition Memory. | Yoo KS et al. | — | 2020 | → |
| The Emerging Role of ATP-Dependent Chromatin Remodeling in Memory and Substance Use Disorders. | López AJ et al. | — | 2020 | → |
| The mechanisms of action of chromatin remodelers and implications in development and disease. | Sahu RK et al. | — | 2020 | → |
| A brief period of sleep deprivation causes spine loss in the dentate gyrus of mice. | Raven F et al. | — | 2019 | → |
| ACTL6A interacts with p53 in acute promyelocytic leukemia cell lines to affect differentiation via the Sox2/Notch1 signaling pathway. | Zhong PQ et al. | — | 2019 | → |
| A Syndromic Neurodevelopmental Disorder Caused by Mutations in SMARCD1, a Core SWI/SNF Subunit Needed for Context-Dependent Neuronal Gene Regulation in Flies. | Nixon KCJ et al. | — | 2019 | → |
| Balanced actions of protein synthesis and degradation in memory formation. | Park H et al. | — | 2019 | → |
| Behavioral and Biochemical Implications of Dendrimeric Rivastigmine in Memory-Deficit and Alzheimer's Induced Rodents. | Gothwal A et al. | — | 2019 | → |
| Context-Aware Mouse Behavior Recognition Using Hidden Markov Models. | Jiang Z et al. | — | 2019 | → |
| Differential impacts on multiple forms of spatial and contextual memory in diazepam binding inhibitor knockout mice. | Ujjainwala AL et al. | — | 2019 | → |
| Epigenetic mechanisms, trauma, and psychopathology: targeting chromatin remodeling complexes. | Bielawski T et al. | — | 2019 | → |
| Facts and hypotheses about the programming of neuroplastic deficits by prenatal malnutrition. | Barra R et al. | — | 2019 | → |
| Genome-Wide Analysis of the Nucleosome Landscape in Individuals with Coffin-Siris Syndrome. | Kalmbach A et al. | — | 2019 | → |
| HDAC3-Mediated Repression of the <i>Nr4a</i> Family Contributes to Age-Related Impairments in Long-Term Memory. | Kwapis JL et al. | — | 2019 | → |
| How the epigenome integrates information and reshapes the synapse. | Campbell RR et al. | — | 2019 | → |
| Individual components of the SWI/SNF chromatin remodelling complex have distinct roles in memory neurons of the <i>Drosophila</i> mushroom body. | Chubak MC et al. | — | 2019 | → |
| Mutations in ACTL6B Cause Neurodevelopmental Deficits and Epilepsy and Lead to Loss of Dendrites in Human Neurons. | Bell S et al. | — | 2019 | → |
| Mutations in ACTL6B, coding for a subunit of the neuron-specific chromatin remodeling complex nBAF, cause early onset severe developmental and epileptic encephalopathy with brain hypomyelination and cerebellar atrophy. | Fichera M et al. | — | 2019 | → |
| New Concerns for Neurocognitive Function during Deep Space Exposures to Chronic, Low Dose-Rate, Neutron Radiation. | Acharya MM et al. | — | 2019 | → |
| Pathogenic homozygous variations in ACTL6B cause DECAM syndrome: Developmental delay, Epileptic encephalopathy, Cerebral Atrophy, and abnormal Myelination. | Yüksel Z et al. | — | 2019 | → |
| Regulation of Central Nervous System Development by Class I Histone Deacetylases. | D'Mello SR | — | 2019 | → |
| Role for Chromatin Remodeling Factor Chd1 in Learning and Memory. | Schoberleitner I et al. | — | 2019 | → |
| Sustained CaMKII Delta Gene Expression Is Specifically Required for Long-Lasting Memories in Mice. | Zalcman G et al. | — | 2019 | → |
| The BAF complex in development and disease. | Alfert A et al. | — | 2019 | → |
| Three-dimensional chromosome architecture and drug addiction. | Chitaman JM et al. | — | 2019 | → |
| ATP-Dependent Chromatin Remodeling During Cortical Neurogenesis. | Sokpor G et al. | — | 2018 | → |
| Chd2 Is Necessary for Neural Circuit Development and Long-Term Memory. | Kim YJ et al. | — | 2018 | → |
| CREST in the Nucleus Accumbens Core Regulates Cocaine Conditioned Place Preference, Cocaine-Seeking Behavior, and Synaptic Plasticity. | Alaghband Y et al. | — | 2018 | → |
| Deleting HDAC3 rescues long-term memory impairments induced by disruption of the neuron-specific chromatin remodeling subunit BAF53b. | Shu G et al. | — | 2018 | → |
| Dentate gyrus mossy cells control spontaneous convulsive seizures and spatial memory. | Bui AD et al. | — | 2018 | → |
| Epigenetic regulation of the circadian gene Per1 contributes to age-related changes in hippocampal memory. | Kwapis JL et al. | — | 2018 | → |
| Glial fibrillary acidic protein levels are associated with global histone H4 acetylation after spinal cord injury in rats. | de Menezes MF et al. | — | 2018 | → |
| Into the Fourth Dimension: Dysregulation of Genome Architecture in Aging and Alzheimer's Disease. | Winick-Ng W et al. | — | 2018 | → |
| Loss of thin spines and small synapses contributes to defective hippocampal function in aged mice. | Xu B et al. | — | 2018 | → |
| Mechanistic Insights Into MicroRNA-Induced Neuronal Reprogramming of Human Adult Fibroblasts. | Lu YL et al. | — | 2018 | → |
| MeCP2 isoform e1 mutant mice recapitulate motor and metabolic phenotypes of Rett syndrome. | Vogel Ciernia A et al. | — | 2018 | → |
| MicroRNAs Overcome Cell Fate Barrier by Reducing EZH2-Controlled REST Stability during Neuronal Conversion of Human Adult Fibroblasts. | Lee SW et al. | — | 2018 | → |
| Mushroom Body Specific Transcriptome Analysis Reveals Dynamic Regulation of Learning and Memory Genes After Acquisition of Long-Term Courtship Memory in <i>Drosophila</i>. | Jones SG et al. | — | 2018 | → |
| The chromatin basis of neurodevelopmental disorders: Rethinking dysfunction along the molecular and temporal axes. | Gabriele M et al. | — | 2018 | → |
| UBE3A-mediated p18/LAMTOR1 ubiquitination and degradation regulate mTORC1 activity and synaptic plasticity. | Sun J et al. | — | 2018 | → |
| Ablation of BAF170 in Developing and Postnatal Dentate Gyrus Affects Neural Stem Cell Proliferation, Differentiation, and Learning. | Tuoc T et al. | — | 2017 | → |
| Arid1b haploinsufficiency disrupts cortical interneuron development and mouse behavior. | Jung EM et al. | — | 2017 | → |
| BAF53b, a Neuron-Specific Nucleosome Remodeling Factor, Is Induced after Learning and Facilitates Long-Term Memory Consolidation. | Yoo M et al. | — | 2017 | → |
| Chromatin Remodeling BAF (SWI/SNF) Complexes in Neural Development and Disorders. | Sokpor G et al. | — | 2017 | → |
| Distinct roles for the deacetylase domain of HDAC3 in the hippocampus and medial prefrontal cortex in the formation and extinction of memory. | Alaghband Y et al. | — | 2017 | → |
| Early motor phenotype detection in a female mouse model of Rett syndrome is improved by cross-fostering. | Vogel Ciernia A et al. | — | 2017 | → |
| Evidence for opposing roles of Celsr3 and Vangl2 in glutamatergic synapse formation. | Thakar S et al. | — | 2017 | → |
| Exonic Mosaic Mutations Contribute Risk for Autism Spectrum Disorder. | Krupp DR et al. | — | 2017 | → |
| Global loss of acetylcholinesterase activity with mitochondrial complexes inhibition and inflammation in brain of hypercholesterolemic mice. | Paul R et al. | — | 2017 | → |
| Learning in the machine: The symmetries of the deep learning channel. | Baldi P et al. | — | 2017 | → |
| Mutation of neuron-specific chromatin remodeling subunit BAF53b: rescue of plasticity and memory by manipulating actin remodeling. | Vogel Ciernia A et al. | — | 2017 | → |
| Regulation of BAZ1A and nucleosome positioning in the nucleus accumbens in response to cocaine. | Sun H et al. | — | 2017 | → |
| The SWI/SNF subunit Bcl7a contributes to motor coordination and Purkinje cell function. | Wischhof L et al. | — | 2017 | → |
| Transcribing the connectome: roles for transcription factors and chromatin regulators in activity-dependent synapse development. | Chen LF et al. | — | 2017 | → |
| Variation in SWI/SNF Chromatin Remodeling Complex Proteins is Associated with Alcohol Dependence and Antisocial Behavior in Human Populations. | Mathies LD et al. | — | 2017 | → |
| A theory of local learning, the learning channel, and the optimality of backpropagation. | Baldi P et al. | — | 2016 | → |
| ATP-dependent chromatin remodeling during mammalian development. | Hota SK et al. | — | 2016 | → |
| Autism-Associated Chromatin Regulator Brg1/SmarcA4 Is Required for Synapse Development and Myocyte Enhancer Factor 2-Mediated Synapse Remodeling. | Zhang Z et al. | — | 2016 | → |
| BAZ1B in Nucleus Accumbens Regulates Reward-Related Behaviors in Response to Distinct Emotional Stimuli. | Sun H et al. | — | 2016 | → |
| BCL11A Haploinsufficiency Causes an Intellectual Disability Syndrome and Dysregulates Transcription. | Dias C et al. | — | 2016 | → |
| BDNF rescues BAF53b-dependent synaptic plasticity and cocaine-associated memory in the nucleus accumbens. | White AO et al. | — | 2016 | → |
| BRG1 in the Nucleus Accumbens Regulates Cocaine-Seeking Behavior. | Wang ZJ et al. | — | 2016 | → |
| Chromatin Remodeling in Addiction: BRG1-SMAD3 Interaction Contributes to Cued Reinstatement of Cocaine Seeking. | Smith AC | — | 2016 | → |
| Converging, Synergistic Actions of Multiple Stress Hormones Mediate Enduring Memory Impairments after Acute Simultaneous Stresses. | Chen Y et al. | — | 2016 | → |
| Deleting both PHLPP1 and CANP1 rescues impairments in long-term potentiation and learning in both single knockout mice. | Liu Y et al. | — | 2016 | → |
| Epigenetic Regulation by ATP-Dependent Chromatin-Remodeling Enzymes: SNF-ing Out Crosstalk. | Runge JS et al. | — | 2016 | → |
| Essential Roles for ARID1B in Dendritic Arborization and Spine Morphology of Developing Pyramidal Neurons. | Ka M et al. | — | 2016 | → |
| Haploinsufficiency of BAZ1B contributes to Williams syndrome through transcriptional dysregulation of neurodevelopmental pathways. | Lalli MA et al. | — | 2016 | → |
| Promoter-Specific Effects of DREADD Modulation on Hippocampal Synaptic Plasticity and Memory Formation. | López AJ et al. | — | 2016 | → |
| Sleep deprivation causes memory deficits by negatively impacting neuronal connectivity in hippocampal area CA1. | Havekes R et al. | — | 2016 | → |
| The Many Roles of BAF (mSWI/SNF) and PBAF Complexes in Cancer. | Hodges C et al. | — | 2016 | → |
| The potential of epigenetics in stress-enhanced fear learning models of PTSD. | Blouin AM et al. | — | 2016 | → |
| Where Environment Meets Cognition: A Focus on Two Developmental Intellectual Disability Disorders. | De Toma I et al. | — | 2016 | → |
| ACF chromatin-remodeling complex mediates stress-induced depressive-like behavior. | Sun H et al. | — | 2015 | → |
| A novel, long-lived, and highly engraftable immunodeficient mouse model of mucopolysaccharidosis type I. | Mendez DC et al. | — | 2015 | → |
| Camk2a-Cre-mediated conditional deletion of chromatin remodeler Brg1 causes perinatal hydrocephalus. | Cao M et al. | — | 2015 | → |
| Early postnatal nicotine exposure causes hippocampus-dependent memory impairments in adolescent mice: Association with altered nicotinic cholinergic modulation of LTP, but not impaired LTP. | Nakauchi S et al. | — | 2015 | → |
| Epigenetics and therapeutic targets mediating neuroprotection. | Qureshi IA et al. | — | 2015 | → |
| Genotype to phenotype relationships in autism spectrum disorders. | Chang J et al. | — | 2015 | → |
| How data analysis affects power, reproducibility and biological insight of RNA-seq studies in complex datasets. | Peixoto L et al. | — | 2015 | → |
| Impaired Contextual Fear Extinction Learning is Associated with Aberrant Regulation of CHD-Type Chromatin Remodeling Factors. | Wille A et al. | — | 2015 | → |
| Loss of BAF (mSWI/SNF) Complexes Causes Global Transcriptional and Chromatin State Changes in Forebrain Development. | Narayanan R et al. | — | 2015 | → |
| Mammalian SWI/SNF chromatin remodeling complexes and cancer: Mechanistic insights gained from human genomics. | Kadoch C et al. | — | 2015 | → |
| Neuroepigenomics: Resources, Obstacles, and Opportunities. | Satterlee JS et al. | — | 2015 | → |
| Nucleosome Repositioning: A Novel Mechanism for Nicotine- and Cocaine-Induced Epigenetic Changes. | Brown AN et al. | — | 2015 | → |
| Role of nucleosome remodeling in neurodevelopmental and intellectual disability disorders. | López AJ et al. | — | 2015 | → |
| Role of Tet1 and 5-hydroxymethylcytosine in cocaine action. | Feng J et al. | — | 2015 | → |
| SWI/SNF chromatin remodeling regulates alcohol response behaviors in Caenorhabditis elegans and is associated with alcohol dependence in humans. | Mathies LD et al. | — | 2015 | → |
| The epigenetics of aging and neurodegeneration. | Lardenoije R et al. | — | 2015 | → |
| The L-type calcium channel Cav1.3 is required for proper hippocampal neurogenesis and cognitive functions. | Marschallinger J et al. | — | 2015 | → |
| The Transcription Repressor REST in Adult Neurons: Physiology, Pathology, and Diseases | Baldelli P et al. | — | 2015 | → |
| Toward understanding the role of the neuron-specific BAF chromatin remodeling complex in memory formation. | Choi KY et al. | — | 2015 | → |
| Up-regulation of HP1γ expression during neuronal maturation promotes axonal and dendritic development in mouse embryonic neocortex. | Oshiro H et al. | — | 2015 | → |
| An evolving view of epigenetic complexity in the brain. | Qureshi IA et al. | — | 2014 | → |
| Coffin-Siris syndrome and related disorders involving components of the BAF (mSWI/SNF) complex: historical review and recent advances using next generation sequencing. | Kosho T et al. | — | 2014 | → |
| Conserved higher-order chromatin regulates NMDA receptor gene expression and cognition. | Bharadwaj R et al. | — | 2014 | → |
| Does stress remove the HDAC brakes for the formation and persistence of long-term memory? | White AO et al. | — | 2014 | → |
| Epigenetic mechanisms in fear conditioning: implications for treating post-traumatic stress disorder. | Kwapis JL et al. | — | 2014 | → |
| Epigenetic mechanisms of memory formation and reconsolidation. | Jarome TJ et al. | — | 2014 | → |
| Epigenetics across the human lifespan. | Kanherkar RR et al. | — | 2014 | → |
| Examining object location and object recognition memory in mice. | Vogel-Ciernia A et al. | — | 2014 | → |
| Neuron-specific chromatin remodeling: a missing link in epigenetic mechanisms underlying synaptic plasticity, memory, and intellectual disability disorders. | Vogel-Ciernia A et al. | — | 2014 | → |
| Object-location training elicits an overlapping but temporally distinct transcriptional profile from contextual fear conditioning. | Poplawski SG et al. | — | 2014 | → |
| Prefrontal consolidation supports the attainment of fear memory accuracy. | Vieira PA et al. | — | 2014 | → |
| Reduced cognition in Syngap1 mutants is caused by isolated damage within developing forebrain excitatory neurons. | Ozkan ED et al. | — | 2014 | → |
| Regulating the chromatin landscape: structural and mechanistic perspectives. | Bartholomew B | — | 2014 | → |
| Roles of chromatin remodeling BAF complex in neural differentiation and reprogramming. | Narayanan R et al. | — | 2014 | → |
| Snf2h-mediated chromatin organization and histone H1 dynamics govern cerebellar morphogenesis and neural maturation. | Alvarez-Saavedra M et al. | — | 2014 | → |
| The future of neuroepigenetics in the human brain. | Mitchell A et al. | — | 2014 | → |
| The histone acetyltransferase MOF activates hypothalamic polysialylation to prevent diet-induced obesity in mice. | Brenachot X et al. | — | 2014 | → |
| The role of BAF (mSWI/SNF) complexes in mammalian neural development. | Son EY et al. | — | 2014 | → |
| Transcriptional co-repressors and memory storage. | Schoch H et al. | — | 2014 | → |
| Autism genes keep turning up chromatin. | Lasalle JM | — | 2013 | → |
| Creating a neural specific chromatin landscape by npBAF and nBAF complexes. | Staahl BT et al. | — | 2013 | → |
| CRESTing the ALS mountain. | Renton AE et al. | — | 2013 | → |
| Epigenetic layers and players underlying neurodevelopment. | LaSalle JM et al. | — | 2013 | → |
| Epigenetics of neural repair following spinal cord injury. | York EM et al. | — | 2013 | → |
| Reprogramming human fibroblasts to neurons by recapitulating an essential microRNA-chromatin switch. | Tang J et al. | — | 2013 | → |