Cellular distribution of the calcium binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns

The three calcium-binding proteins parvalbumin, calbindin, and calretinin a re found in morphologically distinct classes of inhibitory interneurons as well as in some pyramidal neurons in the mammalian neocortex. Although ther e is a wide variability in the qualitative and quantitative characteristics of the neocortical subpopulations of calcium-binding protein-immunoreactiv e neurons in mammals, most of the available data show that there is a funda mental similarity among the mammalian species investigated so far, in terms of the distribution of parvalbumin, calbindin, and calretinin across the d epth of the neocortex. Thus, calbindin- and calretinin-immunoreactive neuro ns are predominant in layers II and III, but are present across all cortica l layers, whereas parvalbumin-immunoreactive neurons are more prevalent in the middle and lower cortical layers. These different neuronal populations have well defined regional and laminar distribution, neurochemical characte ristics and synaptic connections, and each of these cell types displays a p articular developmental sequence. Most of the available data on the develop ment, distribution and morphological characteristics of these calcium-bindi ng proteins are from studies in common laboratory animals such as the rat, mouse, cat, macaque monkey, as well as from postmortem analyses in humans, but there are virtually no data on other species aside of a few incidental reports. In the context of the evolution of mammalian neocortex, the distri bution and morphological characteristics of calcium-binding protein-immunor eactive neurons may help defining taxon-specific patterns that may be used as reliable phylogenetic traits. It would be interesting to extend such neu rochemical analyses of neuronal subpopulations to other species to assess t he degree to which neurochemical specialization of particular neuronal subt ypes, as well as their regional and laminar distribution in the cerebral co rtex, may represent sets of derived features in any given mammalian order. This could be particularly interesting in view of the consistent difference s in neurochemical typology observed in considerably divergent orders such as cetaceans and certain families of insectivores and metatherians, as well as in monotremes. The present article provides an overview of calcium-bind ing protein distribution across a large number of representative mammalian species and a review of their developmental patterns in the species where d ata are available. This analysis demonstrates that while it is likely that the developmental patterns are quite consistent across species, at least ba sed on the limited number of species for which ontogenetic data exist, the distribution and morphology of calcium-binding protein-containing neurons v aries substantially among mammalian orders and that certain species show hi ghly divergent patterns compared to closely related taxa. Interestingly, pr imates, carnivores, rodents and tree shrews appear closely related on the b asis of the observed patterns, marsupials show some affinities with that gr oup, whereas prototherians have unique patterns. Our findings also support the relationships of cetaceans and ungulates, and demonstrates possible aff inities between carnivores and ungulates, as well as the existence of commo n, probably primitive, traits in cetaceans and insectivores. (C) 1999 Elsev ier Science B.V. All rights reserved.