TY - JOUR
T1 - Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals
T2 - Phylogenetic and developmental patterns
AU - Hof, Patrick R.
AU - Glezer, Ilya I.
AU - Condé, Françoise
AU - Flagg, Roxana A.
AU - Rubin, Marina B.
AU - Nimchinsky, Esther A.
AU - Vogt Weisenhorn, Daniela M.
N1 - Funding Information:
The authors would like to thank Drs J.M. Allman, C. Bouras, J.M. Erwin, P.J. Gannon, L. Garibaldi, E. Gilissen, S. Kohama, L.A. Krubitzer, T.F. Ladygina, J. Marcus, A.M. Mass, J. McCoy, S. McFadden, G. Meyer, E.J. Mufson, D.P. Perl, A.V. Revishchin, S. Ridgway, A. Ya. Supin, L.G. Ungerleider, and J. Zook for generously providing many of the specimens included in these studies, Drs M.R. Celio, P.J. Morgane, and J.H. Morrison, for their constant interest and support, B. Schwaller for discussion, and M.M. Adams, W.G.M. Janssen, A.P. Leonard, F. Robenzadeh, and G. Yeung for expert technical assistance. Supported in part by PSC-CUNY grant 662232, DFG grant Vo724/1-1, NIH Human Brain Project grant MHDA52154, Mount Sinai School of Medicine, and the Swiss Academy of Natural Science.
PY - 1999/2
Y1 - 1999/2
N2 - The three calcium-binding proteins parvalbumin, calbindin, and calretinin are found in morphologically distinct classes of inhibitory interneurons as well as in some pyramidal neurons in the mammalian neocortex. Although there is a wide variability in the qualitative and quantitative characteristics of the neocortical subpopulations of calcium-binding protein- immunoreactive neurons in mammals, most of the available data show that there is a fundamental similarity among the mammalian species investigated so far, in terms of the distribution of parvalbumin, calbindin, and calretinin across the depth of the neocortex. Thus, calbindin- and calretinin-immunoreactive neurons are predominant in layers II and III, but are present across all cortical 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 characteristics and synaptic connections, and each of these cell types displays a particular developmental sequence. Most of the available data on the development, distribution and morphological characteristics of these calcium-binding 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 distribution and morphological characteristics of calcium-binding protein-immunoreactive neurons may help defining taxon- specific patterns that may be used as reliable phylogenetic traits. It would be interesting to extend such neurochemical analyses of neuronal subpopulations to other species to assess the degree to which neurochemical specialization of particular neuronal subtypes, as well as their regional and laminar distribution in the cerebral cortex, may represent sets of derived features in any given mammalian order. This could be particularly interesting in view of the consistent differences 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-binding protein distribution across a large number of representative mammalian species and a review of their developmental patterns in the species where data are available. This analysis demonstrates that while it is likely that the developmental patterns are quite consistent across species, at least based on the limited number of species for which ontogenetic data exist, the distribution and morphology of calcium-binding protein-containing neurons varies substantially among mammalian orders and that certain species show highly divergent patterns compared to closely related taxa. Interestingly, primates, carnivores, rodents and tree shrews appear closely related on the basis of the observed patterns, marsupials show some affinities with that group, whereas prototherians have unique patterns. Our findings also support the relationships of cetaceans and ungulates, and demonstrates possible affinities between carnivores and ungulates, as well as the existence of common, probably primitive, traits in cetaceans and insectivores.
AB - The three calcium-binding proteins parvalbumin, calbindin, and calretinin are found in morphologically distinct classes of inhibitory interneurons as well as in some pyramidal neurons in the mammalian neocortex. Although there is a wide variability in the qualitative and quantitative characteristics of the neocortical subpopulations of calcium-binding protein- immunoreactive neurons in mammals, most of the available data show that there is a fundamental similarity among the mammalian species investigated so far, in terms of the distribution of parvalbumin, calbindin, and calretinin across the depth of the neocortex. Thus, calbindin- and calretinin-immunoreactive neurons are predominant in layers II and III, but are present across all cortical 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 characteristics and synaptic connections, and each of these cell types displays a particular developmental sequence. Most of the available data on the development, distribution and morphological characteristics of these calcium-binding 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 distribution and morphological characteristics of calcium-binding protein-immunoreactive neurons may help defining taxon- specific patterns that may be used as reliable phylogenetic traits. It would be interesting to extend such neurochemical analyses of neuronal subpopulations to other species to assess the degree to which neurochemical specialization of particular neuronal subtypes, as well as their regional and laminar distribution in the cerebral cortex, may represent sets of derived features in any given mammalian order. This could be particularly interesting in view of the consistent differences 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-binding protein distribution across a large number of representative mammalian species and a review of their developmental patterns in the species where data are available. This analysis demonstrates that while it is likely that the developmental patterns are quite consistent across species, at least based on the limited number of species for which ontogenetic data exist, the distribution and morphology of calcium-binding protein-containing neurons varies substantially among mammalian orders and that certain species show highly divergent patterns compared to closely related taxa. Interestingly, primates, carnivores, rodents and tree shrews appear closely related on the basis of the observed patterns, marsupials show some affinities with that group, whereas prototherians have unique patterns. Our findings also support the relationships of cetaceans and ungulates, and demonstrates possible affinities between carnivores and ungulates, as well as the existence of common, probably primitive, traits in cetaceans and insectivores.
KW - Brain development
KW - Brain evolution
KW - Carnivores
KW - Cerebral cortex
KW - Cetaceans
KW - Chemoarchitecture
KW - Interneurons
KW - Mammalian brain
KW - Marsupials
KW - Monotremes
KW - Primates
KW - Rodents
KW - Ungulates
KW - Whales
UR - http://www.scopus.com/inward/record.url?scp=0032942714&partnerID=8YFLogxK
U2 - 10.1016/S0891-0618(98)00065-9
DO - 10.1016/S0891-0618(98)00065-9
M3 - Review article
C2 - 10223310
AN - SCOPUS:0032942714
SN - 0891-0618
VL - 16
SP - 77
EP - 116
JO - Journal of Chemical Neuroanatomy
JF - Journal of Chemical Neuroanatomy
IS - 2
ER -