Calcium‐binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex

Abstract

Recent studies have shown that the presence of immunoreactivity for parvalbumin (PV-IR) and calbindin-D 28k (Cal-IR) can be used as markers for certain types of gamma-aminobutyric acid (GABA) immunoreactive interneurons in monkey cerebral cortex. Little quantitative information is available regarding the features that distinguish these two subpopulations, however. Therefore, in this study we localized PV-IR and Cal-IR neurons in Macaca monkey striate cortex and analyzed quantitatively their laminar distribution, cell morphology, and co-localization with GABA by double-labeling immunocytochemistry. PV-IR was found in nonpyramidal cells in all layers of the cortex, although PV-IR cells in layer 1 were rare. In contrast, Cal-IR was found mainly in nonpyramidal cells in two bands corresponding to layers 2-3 and 5-6. We found very few double-labeled PV-IR/Cal-IR cells but confirmed that almost all PV-IR and Cal-IR cells are GABAergic. Overall, 74% of GABA neurons in striate cortex displayed PV-IR compared to only 12% that displayed Cal-IR and 14% that were GABA-IR only. Quantitative analysis indicated that the relative proportion of GABA cells that displayed PV-IR or Cal-IR showed conspicuous laminar differences, which were often complementary. Cell size measurements indicated that PV-IR/GABA cells in layers 2-3 and 5-6 were significantly larger than Cal-IR/GABA cells. Analysis of the size, shape, and orientation of stained cell bodies and proximal dendrites further demonstrated that each subpopulation contained several different types of smooth stellate cells, suggesting that Cal-IR and PV-IR are found in functionally and morphologically heterogeneous subpopulations of GABA neurons. There was a thick bundle of PV-IR axons in the white matter underlying the striate but not prestriate cortex. PV-IR punctate labeling matched the cytochrome oxidase staining pattern in layers 4A and 4C, suggesting that PV-IR is present in geniculocortical afferents as well as intrinsic neurons. Cal-IR neuropil staining was high in layers 1, 2, 4B, and 5, where cytochrome oxidase staining is relatively low. We did not find a preferential localization of either PV-IR or Cal-IR cell bodies in any cytochrome oxidase compartments in layers 2-3 of the cortex. These findings indicate that PV and Cal are distributed into different neuronal circuits.

Neurochemical and Structural Organization of the Principal Nucleus of the Inferior Olive in the Human

“…In the cerebellar cortex, CB and PV are found in Purkinje cells (Celio, 1990 for rat and unpublished observations in human cerebellar cortex), whereas CR immunoreactivity is found in unipolar brush cells and Lugaro cells (Floris et al, 1994;Nunzi et al, 2002). In cerebral cortex, NPNFP is seen in projection neurons and is not typically colocalized with calcium-binding proteins (Van Brederode et al, 1990;Glezer et al, 1993;Hof and Morrison, 1995;Hof et al, 1996Hof et al, , 1997. One exception is a population of CB-immunoreactive pyramidal neurons in cortical layers II and III (Hof and Morrison, 1991;Hayes and Lewis, 1992;Kondo et al, 1999) and another is CR-immunoreactive pyramidal neurons in human and great ape anterior cingulate cortex (Hof et al, 2001).…”

Contrast Dependence and Differential Contributions from Somatostatin- and Parvalbumin-Expressing Neurons to Spatial Integration in Mouse V1

“…Another important difference in the monkey is the distributions of different types of interneurons. Although SOM ϩ neurons are present across layers in macaque V1 (Hendry et al, 1984;Campbell et al, 1987), they are sparse (Hendry et al, 1984) and the proportion of PV ϩ interneurons is higher in the monkey, ϳ74% (Van Brederode et al, 1990) compared with ϳ40% in the mouse (Xu et al, 2010). It is therefore unclear whether the effect of PV ϩ and SOM ϩ neurons on spatial integration is similar in other species such as the monkey.…”

Immunoreactivity for calcium-binding proteins defines subregions of the vestibular nuclear complex of the cat

“…Purkinje cells, which are GABAergic, do not contain calretinin (Arai et al 1991;Résibois and Rogers 1992;Rogers and Résibois 1992;Edmonds et al 2000), and do colocalize parvalbumin and calbindin (Batini 1990;Celio 1990). In cerebral cortex each calcium-binding protein is found in a separate population of GABAergic interneurons (Van Brederode et al 1990), and in the vestibular nerve, the three proteins are present in three different populations of glutamatergic fibers (Carpenter et al 1990). Physiological roles of the different calcium-binding proteins are still debated (Arai et al 1991;Baimbridge et al 1992;Rogers and Résibois 1992).…”