Estimating the heritability of psychological measures in the Human Connectome Project dataset

The Human Connectome Project (HCP) is a large structural and functional MRI dataset with a rich array of behavioral measures and extensive family structure. This makes it a valuable resource for investigating questions about individual differences, including questions about heritability. While its MRI data have been analyzed extensively in this regard, to our knowledge a comprehensive estimation of the heritability of the behavioral dataset has never been conducted. Using a set of behavioral measures of personality, emotion and cognition, we show that it is possible to re-identify the same individual across two testing times, and identify identical twins. Using machine-learning (univariate linear model, Ridge classifier and Random Forest model) we estimated the heritability of 37 behavioral measures and compared the results to those derived from twin correlations. Correlations between the standard heritability metric and each set of model weights ranged from 0.42 to 0.67, and questionnaire-based and task-based measures did not differ significantly in their heritability. We further derived nine latent factors from the 37 measures and repeated the heritability estimation; in this case, the correlations between the standard heritability and each set of model weights were lower, ranging from 0.15 to 0.38. One specific discrepancy arose for the general intelligence factor, which all models assigned high importance, but the standard heritability calculation did not. We present an alternative method for qualitatively estimating the heritability of the behavioral measures in the HCP as a resource for other investigators, and recommend the use of machine-learning models for estimating heritability.

[1]  Fernando E Boada,et al.  Mapping brain–behavior networks using functional and structural connectome fingerprinting in the HCP dataset , 2019, Brain and behavior.

[2]  T. Braver,et al.  Pattern similarity analyses of frontoparietal task coding: Individual variation and genetic influences , 2019, bioRxiv.

[3]  Lachlan T. Strike,et al.  Genetic Complexity of Cortical Structure: Differences in Genetic and Environmental Factors Influencing Cortical Surface Area and Thickness , 2019, Cerebral cortex.

[4]  Nikolaus Kriegeskorte,et al.  Interpreting encoding and decoding models , 2018, Current Opinion in Neurobiology.

[5]  Bing Liu,et al.  Genetic influences on cortical myelination in the human brain , 2018, Genes, brain, and behavior.

[6]  D. Collins,et al.  Neurobehavioral correlates of obesity are largely heritable , 2017, Proceedings of the National Academy of Sciences.

[7]  C. Pallier,et al.  Shared genetic aetiology between cognitive performance and brain activations in language and math tasks , 2018, Scientific Reports.

[8]  Vincent Frouin,et al.  Genetic Influence on the Sulcal Pits: On the Origin of the First Cortical Folds , 2018, Cerebral cortex.

[9]  Chao Zhang,et al.  Functional connectivity predicts gender: Evidence for gender differences in resting brain connectivity , 2018, Human brain mapping.

[10]  Paola Galdi,et al.  Resting-State Functional Brain Connectivity Best Predicts the Personality Dimension of Openness to Experience , 2018, Personality Neuroscience.

[11]  Yong He,et al.  Chronnectome fingerprinting: Identifying individuals and predicting higher cognitive functions using dynamic brain connectivity patterns , 2018, Human brain mapping.

[12]  Oscar Miranda-Dominguez,et al.  Heritability of the human connectome: A connectotyping study , 2017, Network Neuroscience.

[13]  Paul M. Thompson,et al.  Heritability estimates on resting state fMRI data using the ENIGMA analysis pipeline , 2017, PSB.

[14]  Robert King,et al.  An evaluation of machine-learning for predicting phenotype: studies in yeast, rice, and wheat , 2017, Machine Learning.

[15]  K. Wachter,et al.  On Negative Heritability and Negative Estimates of Heritability , 2017, Genetics.

[16]  R. Adolphs,et al.  A new look at domain specificity: insights from social neuroscience , 2017, Nature Reviews Neuroscience.

[17]  Kuldeep Kumar,et al.  Fiberprint: A subject fingerprint based on sparse code pooling for white matter fiber analysis , 2017, NeuroImage.

[18]  D. Meyre,et al.  Assessing the Heritability of Complex Traits in Humans: Methodological Challenges and Opportunities , 2017, Current genomics.

[19]  Thomas E. Nichols,et al.  The heritability of multi-modal connectivity in human brain activity , 2017, eLife.

[20]  Jo Knight,et al.  Heritability of hippocampal subfield volumes using a twin and non‐twin siblings design , 2017, Human brain mapping.

[21]  Mert R. Sabuncu,et al.  Heritability analysis with repeat measurements and its application to resting-state functional connectivity , 2017, Proceedings of the National Academy of Sciences.

[22]  Abbas Babajani-Feremi,et al.  Neural Mechanism Underling Comprehension of Narrative Speech and Its Heritability: Study in a Large Population , 2017, Brain Topography.

[23]  Wei Q. Deng,et al.  A machine-learning heuristic to improve gene score prediction of polygenic traits , 2017, Scientific Reports.

[24]  E. Charney Genes, behavior, and behavior genetics. , 2017, Wiley interdisciplinary reviews. Cognitive science.

[25]  Gilles Blanchard,et al.  Combining Multiple Hypothesis Testing with Machine Learning Increases the Statistical Power of Genome-wide Association Studies , 2016, Scientific Reports.

[26]  Svetha Venkatesh,et al.  Stabilizing Linear Prediction Models Using Autoencoder , 2016, ADMA.

[27]  Tian Ge,et al.  Multidimensional heritability analysis of neuroanatomical shape , 2016, Nature Communications.

[28]  T. Spector,et al.  Genetic and environmental influences on height from infancy to early adulthood: An individual-based pooled analysis of 45 twin cohorts , 2016, Scientific Reports.

[29]  D. Boomsma,et al.  The Prenatal Environment in Twin Studies: A Review on Chorionicity , 2016, Behavior genetics.

[30]  Paul M. Thompson,et al.  The common genetic influence over processing speed and white matter microstructure: Evidence from the Old Order Amish and Human Connectome Projects , 2016, NeuroImage.

[31]  Chorionicity and Heritability Estimates from Twin Studies: The Prenatal Environment of Twins and Their Resemblance Across a Large Number of Traits , 2015, Behavior genetics.

[32]  S. Hägg,et al.  Dominant Genetic Variation and Missing Heritability for Human Complex Traits: Insights from Twin versus Genome-wide Common SNP Models. , 2015, American journal of human genetics.

[33]  M. Chun,et al.  Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity , 2015, Nature Neuroscience.

[34]  P. Groenen,et al.  The Current and Future Use of Ridge Regression for Prediction in Quantitative Genetics , 2015, BioMed research international.

[35]  P. Visscher,et al.  Nature Genetics Advance Online Publication , 2022 .

[36]  Paul M. Thompson,et al.  Medial demons registration localizes the degree of genetic influence over subcortical shape variability: An N= 1480 meta-analysis , 2015, 2015 IEEE 12th International Symposium on Biomedical Imaging (ISBI).

[37]  R Plomin,et al.  Genetics and intelligence differences: five special findings , 2014, Molecular Psychiatry.

[38]  Denis Bratko,et al.  Heritability of personality: A meta-analysis of behavior genetic studies. , 2015, Psychological bulletin.

[39]  Hong Xian,et al.  Genetic and Environmental Influences of General Cognitive Ability: Is g a valid latent construct? , 2014, Intelligence.

[40]  Stefan Haufe,et al.  On the interpretation of weight vectors of linear models in multivariate neuroimaging , 2014, NeuroImage.

[41]  J. Felson,et al.  What can we learn from twin studies? A comprehensive evaluation of the equal environments assumption. , 2014, Social science research.

[42]  Ching Lee Koo,et al.  A Review for Detecting Gene-Gene Interactions Using Machine Learning Methods in Genetic Epidemiology , 2013, BioMed research international.

[43]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[44]  E. Tucker-Drob,et al.  Explaining the Increasing Heritability of Cognitive Ability Across Development , 2013, Psychological science.

[45]  Damaris Zurell,et al.  Collinearity: a review of methods to deal with it and a simulation study evaluating their performance , 2013 .

[46]  Andreas Papassotiropoulos,et al.  Genetics of human episodic memory: dealing with complexity , 2011, Trends in Cognitive Sciences.

[47]  Wei-Yin Loh,et al.  Classification and regression trees , 2011, WIREs Data Mining Knowl. Discov..

[48]  N. Martin,et al.  The heritability of general cognitive ability increases linearly from childhood to young adulthood , 2010, Molecular Psychiatry.

[49]  Robert P. Freckleton,et al.  Dealing with collinearity in behavioural and ecological data: model averaging and the problems of measurement error , 2010, Behavioral Ecology and Sociobiology.

[50]  J. Beckwith,et al.  Twin Studies of Political Behavior: Untenable Assumptions? , 2008, Perspectives on Politics.

[51]  Eric Boerwinkle,et al.  Application of machine learning algorithms to predict coronary artery calcification with a sibship‐based design , 2008, Genetic epidemiology.

[52]  Peter H. Schönemann,et al.  On models and muddles of heritability , 2005, Genetica.

[53]  T. Bouchard,et al.  CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE Genetic Influence on Human Psychological Traits A , 2022 .

[54]  J. Joseph Twin Studies in Psychiatry and Psychology: Science or Pseudoscience? , 2004, Psychiatric Quarterly.

[55]  Jennifer R. Harris,et al.  Heritability of Adult Body Height: A Comparative Study of Twin Cohorts in Eight Countries , 2003, Twin Research.

[56]  A. Goldberger,et al.  Twin studies in behavioral research: a skeptical view. , 2002, Theoretical population biology.

[57]  Shinichi Morishita,et al.  On Classification and Regression , 1998, Discovery Science.

[58]  Christopher M. Bishop,et al.  Classification and regression , 1997 .

[59]  J. Mallet Ecological and Evolutionary Aspects of Insecticide Resistance . By John A. McKenzie. R. G. Landes Co. (Academic Press). 1996. 885 pages. Hard cover. ISBN 0 12 484825 7. , 1996 .

[60]  A. Thapar,et al.  Twins as a Tool of Behavioral Genetics , 1995 .

[61]  T. Bouchard,et al.  Twins as a tool of behavioral genetics : report of the Dahlem Workshop on What Are the Mechanisms Mediating the Genetic and Environmental Determinants of Behavior? Twins as a Tool of Behavioral Genetics, held in Berlin , 17-22 May 1992 , 1993 .

[62]  T. Bouchard,et al.  Twins as a tool of behavioral genetics. , 1993 .

[63]  R. Plomin Behavioral genetics. , 1991, Research publications - Association for Research in Nervous and Mental Disease.

[64]  L J Eaves,et al.  The genetical analysis of covariance structure , 1977, Heredity.

[65]  H. Grüneberg,et al.  Introduction to quantitative genetics , 1960 .