Updated Neuronal Scaling Rules for the Brains of Glires (Rodents/Lagomorphs)

Brain size scales as different functions of its number of neurons across mammalian orders such as rodents, primates, and insectivores. In rodents, we have previously shown that, across a sample of 6 species, from mouse to capybara, the cerebral cortex, cerebellum and the remaining brain structures increase in size faster than they gain neurons, with an accompanying decrease in neuronal density in these structures [Herculano-Houzel et al.: Proc Natl Acad Sci USA 2006;103:12138–12143]. Important remaining questions are whether such neuronal scaling rules within an order apply equally to all pertaining species, and whether they extend to closely related taxa. Here, we examine whether 4 other species of Rodentia, as well as the closely related rabbit (Lagomorpha), conform to the scaling rules identified previously for rodents. We report the updated neuronal scaling rules obtained for the average values of each species in a way that is directly comparable to the scaling rules that apply to primates [Gabi et al.: Brain Behav Evol 2010;76:32–44], and examine whether the scaling relationships are affected when phylogenetic relatedness in the dataset is accounted for. We have found that the brains of the spiny rat, squirrel, prairie dog and rabbit conform to the neuronal scaling rules that apply to the previous sample of rodents. The conformity to the previous rules of the new set of species, which includes the rabbit, suggests that the cellular scaling rules we have identified apply to rodents in general, and probably to Glires as a whole (rodents/lagomorphs), with one notable exception: the naked mole-rat brain is apparently an outlier, with only about half of the neurons expected from its brain size in its cerebral cortex and cerebellum.

[1]  Roberto Lent,et al.  Isotropic Fractionator: A Simple, Rapid Method for the Quantification of Total Cell and Neuron Numbers in the Brain , 2005, The Journal of Neuroscience.

[2]  Andreas Reichenbach,et al.  Size and density of glial and neuronal cells within the cerebral neocortex of various insectivorian species , 1989, Glia.

[3]  Lu Lu,et al.  The genetic control of neocortex volume and covariation with neocortical gene expression in mice , 2009, BMC Neuroscience.

[4]  Partha P. Mitra,et al.  Scalable architecture in mammalian brains , 2001, Nature.

[5]  J. Kaas,et al.  Cellular scaling rules for primate brains , 2007, Proceedings of the National Academy of Sciences.

[6]  R. J. Mullen,et al.  NeuN, a neuronal specific nuclear protein in vertebrates. , 1992, Development.

[7]  L. Krubitzer,et al.  Comparative studies of diurnal and nocturnal rodents: Differences in lifestyle result in alterations in cortical field size and number , 2010, The Journal of comparative neurology.

[8]  M. Remple,et al.  Somatosensory cortex dominated by the representation of teeth in the naked mole-rat brain , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. Martin,et al.  Relative brain size and basal metabolic rate in terrestrial vertebrates , 1981, Nature.

[10]  Diana K. Sarko,et al.  Neuroanatomy Original Research Article Cellular Scaling Rules of Insectivore Brains , 2022 .

[11]  A. Rinderknecht,et al.  The largest fossil rodent , 2008, Proceedings of the Royal Society B: Biological Sciences.

[12]  Laura M Parkes,et al.  Increased gray matter volume of left pars opercularis in male orchestral musicians correlate positively with years of musical performance , 2011, Journal of magnetic resonance imaging : JMRI.

[13]  E. Nevo,et al.  Neuroglobin, cytoglobin, and myoglobin contribute to hypoxia adaptation of the subterranean mole rat Spalax , 2010, Proceedings of the National Academy of Sciences.

[14]  K. Gunderson,et al.  Increased LIS1 expression affects human and mouse brain development , 2009, Nature Genetics.

[15]  J. Kaas,et al.  Cellular Scaling Rules for the Brains of an Extended Number of Primate Species , 2010, Brain, Behavior and Evolution.

[16]  Tal Pupko,et al.  Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades , 2009, BMC Evolutionary Biology.

[17]  Timothy Edward John Behrens,et al.  The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from Macaque monkeys and humans. , 2006, Cerebral cortex.

[18]  R. Baker,et al.  Squirrels: the animal answer guide , 2007 .

[19]  David Penny,et al.  Four new mitochondrial genomes and the increased stability of evolutionary trees of mammals from improved taxon sampling. , 2002, Molecular biology and evolution.

[20]  E. Harley,et al.  Housekeeping genes for phylogenetic analysis of eutherian relationships. , 2006, Molecular biology and evolution.

[21]  M. Pagel A method for the analysis of comparative data , 1992 .

[22]  W. Wilczynski,et al.  Allometry of major CNS divisions: towards a reevaluation of somatic brain-body scaling. , 1986, Brain, behavior and evolution.

[23]  Suzana Herculano-Houzel,et al.  Coordinated Scaling of Cortical and Cerebellar Numbers of Neurons , 2010, Front. Neuroanat..

[24]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  S. Herculano‐Houzel,et al.  Cellular scaling rules for rodent brains , 2006, Proceedings of the National Academy of Sciences.

[26]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[27]  D. Kruska The Effects of Domestication on Brain Size , 2007 .

[28]  H Haug,et al.  Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). , 1987, The American journal of anatomy.

[29]  P. S. Reynolds HOW BIG IS A GIANT? THE IMPORTANCE OF METHOD IN ESTIMATING BODY SIZE OF EXTINCT MAMMALS , 2002 .

[30]  Jon H. Kaas,et al.  Gorilla and Orangutan Brains Conform to the Primate Cellular Scaling Rules: Implications for Human Evolution , 2011, Brain, Behavior and Evolution.

[31]  C. Gissi,et al.  Phylogenetic analyses of complete mitochondrial genome sequences suggest a basal divergence of the enigmatic rodent Anomalurus , 2007, BMC Evolutionary Biology.

[32]  M. Miyamoto,et al.  Phylogenetic assessment of molecular and morphological data for eutherian mammals. , 1999, Systematic biology.

[33]  Jörn Diedrichsen,et al.  Evolution of the cerebellar cortex: The selective expansion of prefrontal-projecting cerebellar lobules , 2010, NeuroImage.

[34]  K A C ELLIOTT,et al.  Activity of acetylcholine system in cerebral cortex of various unanesthetized mammals. , 1952, The American journal of physiology.

[35]  R A Barton,et al.  The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution. , 2003, Journal of human evolution.

[36]  Frederico A. C. Azevedo,et al.  Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled‐up primate brain , 2009, The Journal of comparative neurology.

[37]  E. Douzery,et al.  Rabbits, if anything, are likely Glires. , 2004, Molecular phylogenetics and evolution.

[38]  H. Frahm,et al.  New and revised data on volumes of brain structures in insectivores and primates. , 1981, Folia primatologica; international journal of primatology.

[39]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[40]  M. Sánchez-Villagra,et al.  The Anatomy of the World's Largest Extinct Rodent , 2003, Science.

[41]  L. Marino Absolute brain size: Did we throw the baby out with the bathwater? , 2006, Proceedings of the National Academy of Sciences.

[42]  M. Stanhope,et al.  Local Molecular Clocks in Three Nuclear Genes: Divergence Times for Rodents and Other Mammals and Incompatibility Among Fossil Calibrations , 2003, Journal of Molecular Evolution.

[43]  W. Atchley,et al.  Genetics of Growth Predict Patterns of Brain-Size Evolution , 1985, Science.

[44]  J. B. Levitt,et al.  The use of a novel and simple method of revealing neural fibers to show the regression of the lateral geniculate nucleus in the naked mole-rat (Heterocephalus glaber) , 2006, Brain Research.