Large and fast human pyramidal neurons associate with intelligence

It is generally assumed that human intelligence relies on efficient processing by neurons in our brain. Although grey matter thickness and activity of temporal and frontal cortical areas correlate with IQ scores, no direct evidence exists that links structural and physiological properties of neurons to human intelligence. Here, we find that high IQ scores and large temporal cortical thickness associate with larger, more complex dendrites of human pyramidal neurons. We show in silico that larger dendritic trees enable pyramidal neurons to track activity of synaptic inputs with higher temporal precision, due to fast action potential kinetics. Indeed, we find that human pyramidal neurons of individuals with higher IQ scores sustain fast action potential kinetics during repeated firing. These findings provide the first evidence that human intelligence is associated with neuronal complexity, action potential kinetics and efficient information transfer from inputs to output within cortical neurons.

[1]  Michael J. Taylor,et al.  Sensitivity and specificity of WAIS–III/WMS–III demographically corrected factor scores in neuropsychological assessment , 2001, Journal of the International Neuropsychological Society.

[2]  Brain Development Cooperative Group,et al.  The NIH MRI study of normal brain development , 2006, NeuroImage.

[3]  S. Linnarsson,et al.  Biological annotation of genetic loci associated with intelligence in a meta-analysis of 87,740 individuals , 2019, Molecular Psychiatry.

[4]  P. Vernon Speed of Information Processing and General Intelligence. , 1983 .

[5]  C. D. de Kock,et al.  Layer-specific cholinergic control of human and mouse cortical synaptic plasticity , 2016, Nature Communications.

[6]  D. Wechsler,et al.  Wechsler Adult Intelligence Scale - fourth edition , 2012 .

[7]  K Ikari,et al.  Aging in the Neuropil of Cerebral Cortex– A Quantitative Ultrastructural Study , 1981, Folia psychiatrica et neurologica japonica.

[8]  Rex E. Jung,et al.  Diffusion markers of dendritic density and arborization in gray matter predict differences in intelligence , 2018, Nature Communications.

[9]  Guy Eyal,et al.  Unique membrane properties and enhanced signal processing in human neocortical neurons , 2016, eLife.

[10]  I. Deary,et al.  The relationship between intelligence and reaction time varies with age: Results from three representative narrow-age age cohorts at 30, 50 and 69 years , 2017, Intelligence.

[11]  Idan Segev,et al.  Comprehensive Morpho-Electrotonic Analysis Shows 2 Distinct Classes of L2 and L3 Pyramidal Neurons in Human Temporal Cortex , 2017, Cerebral cortex.

[12]  M. Häusser,et al.  Targeted dendrotomy reveals active and passive contributions of the dendritic tree to synaptic integration and neuronal output , 2007, Proceedings of the National Academy of Sciences.

[13]  Michele Giugliano,et al.  The Impact of Input Fluctuations on the Frequency–Current Relationships of Layer 5 Pyramidal Neurons in the Rat Medial Prefrontal Cortex , 2007, The Journal of Neuroscience.

[14]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[15]  M. Häusser,et al.  Propagation of action potentials in dendrites depends on dendritic morphology. , 2001, Journal of neurophysiology.

[16]  Daniele Linaro,et al.  High Bandwidth Synaptic Communication and Frequency Tracking in Human Neocortex , 2014, PLoS biology.

[17]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[18]  I. Scheffer,et al.  A missense mutation in the neuronal nicotinic acetylcholine receptor α4 subunit is associated with autosomal dominant nocturnal frontal lobe epilepsy , 1995, Nature Genetics.

[19]  Idan Segev,et al.  Dendrites Impact the Encoding Capabilities of the Axon , 2014, The Journal of Neuroscience.

[20]  J. D. de Ruiter The influence of post-mortem fixation delay on the reliability of the Golgi silver impregnation. , 1983, Brain research.

[21]  Michael L. Hines,et al.  The NEURON Book , 2006 .

[22]  J. Jacobs,et al.  Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. , 2001, Cerebral cortex.

[23]  Dmitri B. Chklovskii,et al.  Wiring Optimization in Cortical Circuits , 2002, Neuron.

[24]  G. Elston Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. , 2003, Cerebral cortex.

[25]  D. Wechsler Wechsler Adult Intelligence Scale , 2021, Encyclopedia of Evolutionary Psychological Science.

[26]  J. D. Ruiter The influence of post-mortem fixation delay on the reliability of the Golgi silver impregnation , 1983, Brain Research.

[27]  Idan Segev,et al.  Modeling a layer 4-to-layer 2/3 module of a single column in rat neocortex: Interweaving in vitro and in vivo experimental observations , 2007, Proceedings of the National Academy of Sciences.

[28]  Noah A. Shamosh,et al.  Multiple Bases of Human Intelligence Revealed by Cortical Thickness and Neural Activation , 2008, The Journal of Neuroscience.

[29]  William Bialek,et al.  Neural Coding of Natural Stimuli: Information at Sub-Millisecond Resolution , 2008, PLoS computational biology.

[30]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[31]  Tyrone D. Cannon,et al.  GWAS meta-analysis reveals novel loci and genetic correlates for general cognitive function: a report from the COGENT consortium , 2017, Molecular Psychiatry.

[32]  Alan C. Evans,et al.  Genetic Contributions to Human Brain Morphology and Intelligence , 2006, The Journal of Neuroscience.

[33]  J. DeFelipe,et al.  Microstructure of the neocortex: Comparative aspects , 2002, Journal of neurocytology.

[34]  C. Spearman General intelligence Objectively Determined and Measured , 1904 .

[35]  Claus C Hilgetag,et al.  Bridging Cytoarchitectonics and Connectomics in Human Cerebral Cortex , 2015, The Journal of Neuroscience.

[36]  R. Kahn,et al.  The association between brain volume and intelligence is of genetic origin , 2002, Nature Neuroscience.

[37]  I. Deary,et al.  The neuroscience of human intelligence differences , 2010, Nature Reviews Neuroscience.

[38]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[39]  Arthur W Toga,et al.  Relationships between IQ and regional cortical gray matter thickness in healthy adults. , 2007, Cerebral cortex.

[40]  Stefano Fusi,et al.  The dynamical response properties of neocortical neurons to temporally modulated noisy inputs in vitro. , 2008, Cerebral cortex.

[41]  Anders Holm,et al.  Socioeconomic Position Across the Life Course and Cognitive Ability Later in Life: The Importance of Considering Early Cognitive Ability , 2019, Journal of aging and health.

[42]  Karama S,et al.  Positive association between cognitive ability and cortical thickness in a representative US sample of healthy 6 to 18 year-olds , 2009, NeuroImage.

[43]  Michael A. McDaniel Big-brained people are smarter: A meta-analysis of the relationship between in vivo brain volume and intelligence , 2005 .

[44]  R. Yuste,et al.  Cortical area and species differences in dendritic spine morphology , 2002, Journal of neurocytology.

[45]  Robert Plomin,et al.  Genome-wide association meta-analysis of 78,308 individuals identifies new loci and genes influencing human intelligence , 2017, Nature Genetics.

[46]  Michael L. Hines,et al.  The NEURON Book: Frontmatter , 2006 .

[47]  P. Hof,et al.  Dendritic morphology of pyramidal neurons in the chimpanzee neocortex: regional specializations and comparison to humans. , 2013, Cerebral cortex.

[48]  Tarmo Strenze Intelligence and socioeconomic success: A meta-analytic review of longitudinal research ☆ , 2007 .

[49]  Guy Eyal,et al.  Dendritic and Axonal Architecture of Individual Pyramidal Neurons across Layers of Adult Human Neocortex , 2015, Cerebral cortex.

[50]  Tyrone D. Cannon,et al.  Large-scale cognitive GWAS Meta-Analysis Reveals Tissue-Specific Neural Expression and Potential Nootropic Drug Targets , 2017, bioRxiv.

[51]  Ruben Schmidt,et al.  Linking Macroscale Graph Analytical Organization to Microscale Neuroarchitectonics in the Macaque Connectome , 2014, The Journal of Neuroscience.

[52]  Alan C. Evans,et al.  Positive association between cognitive ability and cortical thickness in a representative US sample of healthy 6 to 18 year-olds , 2009, NeuroImage.

[53]  C. D. de Kock,et al.  Mechanisms Underlying the Rules for Associative Plasticity at Adult Human Neocortical Synapses , 2013, The Journal of Neuroscience.

[54]  Fred Wolf,et al.  Fast Computations in Cortical Ensembles Require Rapid Initiation of Action Potentials , 2013, The Journal of Neuroscience.

[55]  K. Horikawa,et al.  A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates , 1988, Journal of Neuroscience Methods.

[56]  G. Elston,et al.  The Pyramidal Cell in Cognition: A Comparative Study in Human and Monkey , 2001, The Journal of Neuroscience.

[57]  E. Bedel Relationship between , 2009 .

[58]  M. Giugliano,et al.  Dynamical response properties of neocortical neurons to conductance‐driven time‐varying inputs , 2018, The European journal of neuroscience.

[59]  Ian J Deary,et al.  Stability and change in intelligence from age 11 to ages 70, 79, and 87: the Lothian Birth Cohorts of 1921 and 1936. , 2011, Psychology and aging.

[60]  Perry L. Miller,et al.  Twenty years of ModelDB and beyond: building essential modeling tools for the future of neuroscience , 2016, Journal of Computational Neuroscience.

[61]  Ian J. Deary,et al.  The Stability of Intelligence From Age 11 to Age 90 Years , 2013, Psychological science.

[62]  Hans J. Eysenck,et al.  Reaction time and intelligence: a replicated study , 1986 .