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Review
. 2022 Nov;26(11):909-922.
doi: 10.1016/j.tics.2022.08.012. Epub 2022 Sep 15.

Evolution of cortical neurons supporting human cognition

A A Galakhova  1 , S Hunt  1 , R Wilbers  1 , D B Heyer  1 , C P J de Kock  1 , H D Mansvelder  1 , N A Goriounova  2
Affiliations
Review

Evolution of cortical neurons supporting human cognition

A A Galakhova et al. Trends Cogn Sci. 2022 Nov.

Abstract

Human cognitive abilities are generally thought to arise from cortical expansion over the course of human brain evolution. In addition to increased neuron numbers, this cortical expansion might be driven by adaptations in the properties of single neurons and their local circuits. We review recent findings on the distinct structural, functional, and transcriptomic features of human cortical neurons and their organization in cortical microstructure. We focus on the supragranular cortical layers, which showed the most prominent expansion during human brain evolution, and the properties of their principal cells: pyramidal neurons. We argue that the evolutionary adaptations in neuronal features that accompany the expansion of the human cortex partially underlie interindividual variability in human cognitive abilities.

Keywords: cognition; cortical neurons; evolution; human cortex; human pyramidal neurons; intelligence.

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Conflict of interest statement

Declaration of interests No interests are declared.

Figures

Figure 1.
Figure 1.. Gradients in the complexity of pyramidal neurons and their spine numbers.
Gradients follow the functional hierarchy of cortical areas in primate species: neurons at the top of the hierarchy in prefrontal cortex and temporal lobe have the highest complexity and spine number. Neuronal complexity increases both across brain areas within a primate species, and with brain mass across species. Two example L3 pyramidal neurons from the primary visual area (blue) and the inferotemporal cortical area (orange) from macaque monkey are shown left (modified from [39,40], image from Verhoog, M.B, PhD thesis, Vrije Universiteit Amsterdam, 2016). The height of the colored bars drawn inside the various brain areas in the brain cartoons reflects the number of spines found on neurons, scale bar depicted in the bottom right corner. PFC - prefrontal cortex; TE – inferiotemporal cortex; V1 - primary visual cortex; V2 – secondary visual cortex; V4 – visual area 4.
Figure 2.
Figure 2.. Cortical expansion of the human brain
A. Human and mouse brains differ in size and cortical thickness: histology images of two comparable cortical areas in human (middle temporal gyrus, MTG) and mouse (temporal association area, TeA) show proportionally larger supragranular layer. Images from © 2010 Allen Institute for Brain Science. Allen Human Brain Atlas. Available from: human.brain-map.org). B. Supragranular layer thickness is larger in human cortex than other species, both in absolute size (top) as well as relative to the other cortical layers (bottom) (adapted from [46]).
Figure 3,
Figure 3,. Key Figure. Cortical expansion is accompanied by adaptations in pyramidal neuron morphology
Increased L2/L3 size is accompanied by changes in cytoarchitecture of cortical layers and morphological properties of neurons. Human L2/L3 neurons have 3-fold larger and more complex dendrites than mouse or macaque and contain a larger diversity in transcriptomic excitatory neuron types. In mouse cortex, L2/3 contain three distinct transcriptomic types with relatively compact dendritic morphology, and cell body location strictly adhere to layer boundaries. In contrast, human cortical layers 2 and 3 contain five transcriptomic types that show strong diversity in dendrite morphology, with several large dendrite neuron types that are not found in rodents (based on the data from [1,19,47]).
Figure 4.
Figure 4.. Cellular and cortical properties underlying interindividual differences in human intelligence.
The well-documented association of cortical thickness of MTG with IQ scores in healthy individuals [88,92,93] is driven by interindividual differences in the thickness of layers 2 and 3 in human cortex that also associate with IQ scores. Subjects with higher IQ scores (right column in red boxes) have thicker L2/L3 that contains larger neurons with larger cell bodies at lower neuron densities, than subjects with lower IQ scores (left column in blue boxes). Pyramidal neurons in subjects with higher IQ scores (center red box) have larger and more complex dendritic trees, and these neurons can maintain faster action potential rise speed during repeated firing than neurons in cortical L2/L3 of subjects with lower IQ scores (center blue box). Larger dendrites have more dendritic spines and have physically more room to receive synaptic inputs, thereby larger neurons can integrate more information from other neurons. Action potential shape stability supports fast neuronal information processing. Both factors are potentially contributing to cognitive ability and possibly drive the association of IQ scores with activity of MTG areas in fMRI ([93]; Figure based on the data from [16,95]).
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