Calcium-binding protein-containing neuronal populations in mammalian visual cortex: a comparative study in whales, insectivores, bats, rodents, and primates.

Abstract

This study is focused on comparative analysis of gamma-aminobutyric acid-positive (GABAergic) neuronal populations in primary visual cortex of totally aquatic toothed whales and select terrestrial mammals with different evolutionary histories and various ecological adaptations. The distribution of neuronal populations containing the calcium-binding proteins calbindin and parvalbumin, which are recognized markers for the GABAergic neurons in cerebral cortex, is compared in five species of toothed whales and in representatives (one species each) of insectivores, bats, rodents, and primates. Computerized image analysis has shown that overall quantitative characteristics of GABAergic cortical neurons in toothed whales are similar to those in other mammalian orders. Thus, GABA-positive neurons represent 26% of the total population of cortical neurons in the visual cortex of whales. Some 97% of GABA-positive cells contain calcium-binding proteins, which is numerically similar to these parameters found in primates and other mammals. On the other hand, the typology and laminar distribution of calcium-binding protein-containing neurons in the primary visual cortex of five whale species (Delphinapterus leucas, Globicephala melaena, Phocoena phocoena, Stenella coeruleoalba, and Tursiops truncatus) differ significantly from those of primates (Macaca mulatta) and rodents (Rattus rattus) and are similar to those found in insectivorous bats (Eptesicus fuscus) and hedgehogs (Erinaceus europaeus). In whales, bats, and hedgehogs a significant concentration of calbindin-positive, vertically oriented bipolar and bitufted neurons was found in layers I, II, and IIIc/V with their axons arranged in a three-dimensional network. In primates and rodents they are distributed evenly across all cortical layers and are predominantly multipolar or bitufted neurons found in all cortical layers with their axons oriented along the vertical axis of the cortical plate. The parvalbumin-positive neurons in all mammalian species, including toothed whales, are represented by variously sized multipolar non-pyramidal cells. As opposed to all other mammalian species, the major concentrations of parvalbumin-positive neurons in whales are found in layers IIIc/V and VI, whereas in other cortical layers there are only scattered parvalbumin-positive neurons.(ABSTRACT TRUNCATED AT 400 WORDS)