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 gamma-aminobutyric ac id-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. T he 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 insecti vores, bats, rodents, and primates. Computerized image analysis has sh own that overall quantitative characteristics of GABAergic cortical ne urons 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-pos itive cells contain calcium-binding proteins, which is numerically sim ilar to these parameters found in primates and other mammals. On the o ther hand, the typology and laminar distribution of calcium-binding pr otein-containing neurons in the primary visual cortex of five whale sp ecies (Delphinapterus leucas, Globicephala melaena, Phocoena phocoena, Stenella coeruleoalba, and Tursiops truncatus) differ significantly f rom those of primates (Macaca mulatta) and rodents (Rattus rattus) and are similar to those found in insectivorous bats (Eptesicus fuscus) a nd hedgehogs (Erinaceus europaeus). In whales, bats, and hedgehogs a s ignificant concentration of calbindin-positive, vertically oriented bi polar and bitufted neurons was found in layers I, II, and IIIc/V with their axons arranged in a three-dimensional network. In primates and r odents they are distributed evenly across all cortical layers and are predominantly multipolar or bitufted neurons found in all cortical lay ers with their axons oriented along the vertical axis of the cortical plate. The parvalbumin-positive neurons in all mammalian species, incl uding toothed whales, are represented by variously sized multipolar no n-pyramidal cells. As opposed to all other mammalian species, the majo r concentrations of parvalbumin-positive neurons in whales are found i n layers IIIc/V and VI, whereas in other cortical layers there are onl y scattered parvalbumin-positive neurons. Thus, in layers IIIc/V and V I calbindin- and parvalbumin-positive neuronal populations form overla pping 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 parvalb umin-positive cortical neurons. Thus, the cortical calbindin-positive neuronal population is significantly (two to four times) higher relati ve to the parvalbumin-positive population of neurons in whales and evo lutionary conservative mammals (bats and hedgehogs), whereas in phylog enetically progressive mammals (primates) and moderately progressive m ammals (rodents) calbindin- and parvalbumin-positive populations are a pproximately equal in their relative concentrations. These data sugges t that in cetacean primary visual cortex, as well as in primary cortic es of prototypal terrestrial mammals, the calbindin-positive system of neurons is expressed considerably stronger than the parvalbumin syste m.These findings may relate to the absence or incipience (i.e., relati vely poor development) of layer IV and hypertrophy of layers I and II in cetacean and prototypal mammalian sensory neocortices. This, in tur n, suggests several important differences between prototypal and evolu tionary progressive mammalian orders in the organization of neocortica l afferentation. In whales and, to a lesser extent, in archetypal terr estrial mammals calbindin-positive nuclei of the thalamus may send str ong calbindin-positive afferents to calbindin-rich superficial cortica l layers as well as to limited mid-cortical layers, whereas parvalbumi n-positive afferents from the thalamus may be reduced in view of the a bsence or incipience of layer IV.