Genome-wide association analysis links multiple psychiatric liability genes to oscillatory brain activity.
paper
Primary
Public
- Authors
- Smit, Dirk J A; Wright, Margaret J; Meyers, Jacquelyn L; Martin, Nicholas G; Ho, Yvonne Y W; Malone, Stephen M; Zhang, Jian; Burwell, Scott J; Chorlian, David B; de Geus, Eco J C; Denys, Damiaan; Hansell, Narelle K; Hottenga, Jouke-Jan; McGue, Matt; van Beijsterveldt, Catharina E M; Jahanshad, Neda; Thompson, Paul M; Whelan, Christopher D; Medland, Sarah E; Porjesz, Bernice; Lacono, William G; Boomsma, Dorret I
- Year
- 2018
- Journal
- Human brain mapping
- PMID
- 29947131
- DOI
- 10.1002/hbm.24238
- PMCID
- PMC6179948
Oscillatory activity is crucial for information processing in the brain, and has a long history as a biomarker for psychopathology. Variation in oscillatory activity is highly heritable, but current understanding of specific genetic influences remains limited. We performed the largest genome-wide association study to date of oscillatory power during eyes-closed resting electroencephalogram (EEG) across a range of frequencies (delta 1-3.75 Hz, theta 4-7.75 Hz, alpha 8-12.75 Hz, and beta 13-30 Hz) in 8,425 subjects. Additionally, we performed KGG positional gene-based analysis and brain-expression analyses. GABRA2-a known genetic marker for alcohol use disorder and epilepsy-significantly affected beta power, consistent with the known relation between GABA interneuron activity and beta oscillations. Tissue-specific SNP-based imputation of gene-expression levels based on the GTEx database revealed that hippocampal GABRA2 expression may mediate this effect. Twenty-four genes at 3p21.1 were significant for alpha power (FDR q < .05). SNPs in this region were linked to expression of GLYCTK in hippocampal tissue, and GNL3 and ITIH4 in the frontal cortex-genes that were previously implicated in schizophrenia and bipolar disorder. In sum, we identified several novel genetic variants associated with oscillatory brain activity; furthermore, we replicated and advanced understanding of previously known genes associated with psychopathology (i.e., schizophrenia and alcohol use disorders). Importantly, these psychopathological liability genes affect brain functioning, linking the genes' expression to specific cortical/subcortical brain regions.
Figure 1
Quantile‐quantile plots of observed versus expected –log10(p) for delta, theta, alpha, and beta EEG power at the vertex, occipital alpha power, and occipital alpha peak frequency. Red line is the expected null, grey area is the 95% confidence interval. Dashed red line is the Benjamini‐Hochberg FDR q = .05 threshold. Pink dots are meta‐analyzed SNP p values. FDR‐corrected significance is reached for alpha power at Cz. Blue triangles are KGG gene‐based test p values combining SNP effects within gene regions plus 50k base pairs 3′ and 5′ UTR. Many genes reach FDR significance for alpha oscillation power (see Supporting Information Table S2) [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 2
KGG gene‐based test results Manhattan plots for the six EEG traits measured at the vertex electrode (Cz) and occipital (O1/O2). Dashed line is the threshold for genome‐wide significance. Named genes are significant discoveries under FDR q = .05. Only peak findings in the significant region marked with blue vertical lines are shown. A full listing of FDR significant genes is provided in Supporting Information Table S2 [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 3
FUMA (Watanabe et al., 2017) enrichment analysis. The top 500 genes in the occipital alpha analysis are significantly enriched for genes that are up or down regulated in all cortical and subcortical brain tissues from the GTEx database, save cerebellar hemisphere. Other significantly enriched tissues are heart, whole blood, pancreas, tibial nerve, and liver [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 4
MetaXcan gene‐expression results for chromosomes 2 and 3 indicate which positional gene‐based discoveries and which brain tissues may be involved in affecting alpha oscillation power. Uncorrected p‐values are shown, FDR significant discoveries are marked with a dot. Out of the 24 significant genes in region 3p21, GLYCTK associated with alpha power via hippocampal expression, TEX264 via general cortical expression, GNL3 and ITIH4 via hypothalamic expression. Furthermore, IL18R1, IL1RL1, and MTERF4 on chromosome 2 were not discovered in the positional analysis. These genes affected alpha oscillations via the Putamen and Hippocampus, but IL1RL1 and IL18R1 expression in many other tissues just failed to reach the FDR threshold. Note that FDR correction was performed within tissue [Color figure can be viewed at http://wileyonlinelibrary.com]
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| Name | Type |
|---|---|
| 1000 Genomes Project | cohort |
| 3q26 locus local | variant |
| 4q21 microdeletion syndrome local | phenotype |
| 6q22 locus local | variant |
| adipose phenotypes local | phenotype |
| African American | cohort |
| African American ancestry samples local | cohort |
| age group | cohort |
| ALAS1 local | gene |
| alcohol | phenotype |
| alcohol dependence | phenotype |
| alcohol-dependence family cohort local | cohort |
| Alcohol Use Disorder | phenotype |
| alcohol use disorders | phenotype |
| alpha | anatomy |
| alpha beta oscillation power local | phenotype |
| Alpha beta oscillations local | phenotype |
| alpha oscillation power local | phenotype |
| Alpha oscillation power local | phenotype |
| alpha oscillations | phenotype |
| ALPHA_OSCILLATIONS local | phenotype |
| alpha oscillation strength local | phenotype |
| alpha peak frequency | phenotype |
| alpha power | phenotype |
| ancestry principal components | drug |
| anterior cingulate cortex | anatomy |
| anthropometric traits | phenotype |
| asthma | phenotype |
| Atopic dermatitis | phenotype |
| ATOPIC_DERMATITIS local | phenotype |
| Attentional deficits local | phenotype |
| Australia cohort local | cohort |
| autism | phenotype |
| autism spectrum disorder | phenotype |
| behavioral flexibility | phenotype |
| behavioral phenotypes | phenotype |
| behavioral traits | phenotype |
| benzodiazepines | drug |
| Beta | drug |
| beta oscillations | phenotype |
| beta power | phenotype |
| bipolar disorder | phenotype |
| Bipolar EEG local | phenotype |
| blood | drug |
| blood pressure-related traits local | phenotype |
| brain | anatomy |
| brain activity | phenotype |
| brain derived tissues local | anatomy |
| brain oscillations | phenotype |
| brain tissue | anatomy |
| brain volume | anatomy |
| Brisbane Adolescent Twin Study local | cohort |
| caudate nucleus | anatomy |
| CCDC168 local | gene |
| celiac disease | phenotype |
| CELIAC_DISEASE local | phenotype |
| cerebellum | anatomy |
| cerebral brain tissue local | anatomy |
| CEU | cohort |
| CLHC1 local | gene |
| COGA case control local | cohort |
| COGA Case-Control local | cohort |
| COGA European Ancestry Families local | cohort |
| COGA sample | cohort |
| Collaborative Study on the Genetics of Alcoholism (COGA) | cohort |
| Common SNP variants local | variant |
| cortex | anatomy |
| cortical tissue | anatomy |
| Cz | anatomy |
| Cz alpha local | phenotype |
| Cz alpha power local | phenotype |
| Cz beta power local | phenotype |
| Cz delta power local | phenotype |
| delta | phenotype |
| Delta oscillation power local | phenotype |
| delta oscillations | phenotype |
| delta power | phenotype |
| delta theta oscillation power local | phenotype |
| Delta theta oscillation power local | phenotype |
| disease status | phenotype |
| Dlx5 | gene |
| DLX5/6+/− local | variant |
| DLX6 | gene |
| educational attainment | phenotype |
| EEG | phenotype |
| EEG apparatus local | drug |
| EEG parameters | phenotype |
| EEG phenotypes | phenotype |
| EEG traits local | phenotype |
| EEG workgroup local | cohort |
| endophenotype | phenotype |
| ENIGMA | cohort |
| ENIGMA consortium | cohort |
| epilepsy | phenotype |
| eQTLGen Consortium | cohort |
| EUR 1000 Genomes reference set local | cohort |
| European ancestry | cohort |
| European population | cohort |
| facial bone growth retardation local | phenotype |
| fast beta oscillations local | phenotype |
| Fast Fourier Transformation (FFT) local | drug |
| frontal alpha power local | phenotype |
| frontal cortex | anatomy |
| functional connectivity | phenotype |
| GABA | phenotype |
| GABAA receptor | drug |
| GABRA2 | gene |
| Gabra4 | gene |
| GABRB1 | gene |
| Gabrg1 | gene |
| gamma oscillations | phenotype |
| gene-expression enrichment local | phenotype |
| genes | gene |
| Genotyping platforms local | drug |
| GLT8D1 | gene |
| GLYCTK local | gene |
| GLYTCK local | gene |
| GNL3 | gene |
| growth retardation | phenotype |
| GTEx | cohort |
| HapMap | cohort |
| health | phenotype |
| heart | anatomy |
| heart rate | phenotype |
| heritability | phenotype |
| hippocampus | anatomy |
| hypothalamus | anatomy |
| IBS | cohort |
| IL18R1 | gene |
| IL1RL1 local | gene |
| ILAE Consortium local | cohort |
| imputation algorithms | drug |
| intelligence | phenotype |
| intergenic SNPs at 3q26 local | variant |
| intergenic SNPs at 6q22 local | variant |
| intracranial volume | anatomy |
| Irritable Bowel Syndrome local | phenotype |
| ITIH4 | gene |
| LD Hub | cohort |
| LINC00996 local | gene |
| liver | anatomy |
| LOC101928942 local | gene |
| MATLAB local | drug |
| mental retardation | phenotype |
| METTL21C local | gene |
| movement-prohibitive role local | phenotype |
| MTERF4 local | gene |
| MTFS | cohort |
| Native American ancestry samples local | cohort |
| Netherlands cohort local | cohort |
| Netherlands Twin Register | cohort |
| neurodevelopmental disorder | phenotype |
| Neuropsychiatric and behavioral traits local | phenotype |
| neuropsychiatric disorders | phenotype |
| neuropsychological symptoms local | phenotype |
| neuroticism | phenotype |
| NTR | cohort |
| nucleus accumbens | anatomy |
| occipital alpha local | anatomy |
| occipital alpha power local | phenotype |
| Occipital alpha power local | phenotype |
| occipital cortex | anatomy |
| Occipital (O1, O2) local | anatomy |
| Oscillatory power local | phenotype |
| pancreas | anatomy |
| Parkinson's disease | phenotype |
| patients | cohort |
| PCNX2 local | gene |
| population-based twin cohort local | cohort |
| posterior region | anatomy |
| PRKG2 local | gene |
| psychiatric disorders | phenotype |
| Psychiatric Genomics Consortium | cohort |
| psychiatric traits | phenotype |
| putamen | anatomy |
| QC protocols local | drug |
| QIMR BATS local | cohort |
| Resting state EEG local | phenotype |
| resting-state EEG beta power local | phenotype |
| rs10231372 local | variant |
| rs10910665 local | variant |
| rs11677128 local | variant |
| rs17055223 local | variant |
| rs6867021 local | variant |
| rs7614727 local | variant |
| rs9514041 local | variant |
| rs984924 local | variant |
| saliva | drug |
| schizophrenia | phenotype |
| sex | phenotype |
| SGIP1 | gene |
| skeletal symptoms local | phenotype |
| SNP | cohort |
| speech retardation local | phenotype |
| study cohort | cohort |
| subcortical regions | anatomy |
| subcortical volumes | anatomy |
| Subjective Wellbeing local | phenotype |
| substance use | phenotype |
| subthalamic nucleus | anatomy |
| TEX264 local | gene |
| theta band | phenotype |
| Theta oscillation power local | phenotype |
| theta oscillations | phenotype |
| tibial nerve | anatomy |
| TPP2 local | gene |
| transgenic mice | cohort |
| twin/family studies local | cohort |
| US cohort local | cohort |
| vertex | anatomy |
| Vertex (Cz) local | anatomy |
| WDR82 local | gene |
| whole blood | anatomy |
| young adult samples local | cohort |
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