The Glia-Neuron Index in the Neocortex of Cetartiodactyla and Afrotheria: Implications for Mammalian Brain Evolution
Abstract
Glial cells (astrocytes and oligodendrocytes) play a fundamental role in many brain functions such as propagation of axon potential, integration of neuronal inputs, modulation of synaptic activity and synaptic strength, modulation of glucose metabolism and extracellular ion concentrations, as well as regulation of synaptogenesis and neurogenesis.3,7,8,9,10 Glial cell dysfunction is involved in many neurodegenerative diseases in human.5 However, the number of glial cells in the brain and its relation to the number of neurons, brain size, and neuronal size remains poorly understood. Although several estimates of the glia-neuron index (GNI) are available for a number of mammals, GNI values from cetaceans are few and were obtained with different techniques from different cortical regions, and are therefore not comparable.1,2,4,6 We report GNI values obtained by stereologic techniques, in the anterior cingulate (ACC) and primary somatosensory (S1) cortices of cetaceans encompassing a wide range of brain and body sizes including the bottlenose dolphin (Tursiops truncatus), the Risso's dolphin (Grampus griseus), the harbor porpoise (Phocoena phocoena), the beluga whale (Delphinapterus leucas), the killer whale (Orcinus orca), the dwarf sperm whale (Kogia simus), the sperm whale (Physeter macrocephalus), the humpback whale (Megaptera novaeangliae) and the minke whale (Balaenoptera acutorostrata). The brains of the pigmy hippopotamus (Hexaprotodon liberiensis), manatee (Trichecus manatus), African elephant (Loxodonta africana), and rock hyrax (Procavia capensis) were used for comparative purposes. Our results show that the thick, neuron-poor layer I influences strongly the GNI in Cetartiodactyla. GNI values vary from 3.54 in the harbor porpoise to 13.19 in the sperm whale. In Afrotheria, the GNI values range from 1.18 in the rock hyrax to 4.93 in the African elephant. Of note, these values from large-brained mammals are generally larger than those reported in various neocortical regions of humans (0.68 to 2.19) and macaque monkeys (0.49 to 1). The large variation of GNI values observed among the species investigated in the present study suggests that the ratio of glial cells to neurons does not represent a conservative feature of the mammalian brain, as previously suggested, and that different values of GNI evolved in different taxa possibly in relation to brain size, neuronal size, and metabolic needs.
Acknowledgements
The authors thank Drs. P.J. Morgane and I.I. Glezer for generous donation of the humpback whale and beluga whale brain specimens, Dr. H.H. Oelschläger for donation of the harbor porpoise brain samples, and the Mediterranean Marine Mammals Tissue Bank of the University of Padova for provision of material from the bottlenose dolphin and Risso's dolphins. Sponsored by The James S. McDonnell Foundation; Grant number 22002078 to PRH.
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