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

This study is focused on comparative analysis of γ-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, Phoeoana phocoena, Stenella coeruleoalba, and Tursiops truncates) differ significantly from those of primates (Macaea 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. Thus, in layers IIIc/V and VI calbindin and parvalbumin-positive neuronal populations form overlapping populations. In other mammalian species the parvalbumin-positive neurons are distributed more evenly between different cortical layers. The other prominent difference between mammalian orders was found in the quantitative relationships between calbindin-positive and parvalbumin-positive cortical neurons. Thus, the cortical calbindin-positive neuronal population is significantly (two to four times) higher relative to the parvalbumin-positive population of neurons in whales and evolutionary conservative mammals (bats and hedgehogs), whereas in phylogenetically progressive mammals (primates) and moderately progressive mammals (rodents) calbindin- and parvalbumin-positive populations are approximately equal in their relative concentrations. These data suggest that in cetacean primary visual cortex, as well as in primary cortices of prototypal terrestrial mammals, the calbindin-positive system of neurons is expressed considerably stronger than the parvalbumin system. These findings may relate to the absence or incipience (i.e., relatively poor development) of layer IV and hypertrophy of layers I and II in cetacean and prototypal mammalian sensory neocortices. This, in turn, suggests several important differences between prototypal and evolutionary progressive mammalian orders in the organization of neocortical afferentation. In whales and, to a lesser extent, in archotypal terrestrial mammals calbindin-positive nuclei of the thalamus may send strong calbindin-positive afferents to calbindin-rich superficial cortical layers as well as to limited midcortical layers, whereas parvalbumin-positive afferents from the thalamus may be reduced in view of the absence or incipience of layer IV.