Neurochemical compartmentation of monkey and human visual cortex: Similarities and variations in calbindin immunoreactivity across species

Abstract

The compartmental organization of visual cortical neurons was examined across species of primates by directly comparing the pattern of immunoreactivity for the 28-kD vitamin D-dependent calcium-binding protein (calbindin) in area 17 of squirrel monkeys, macaques, and neurologically normal adult humans. Area 17 of macaques and squirrel monkeys was similar in that somata and processes intensely immunoreactive for calbindin were present in the same layers (II-III, IVB, and V) and in both species formed a well-stained matrix that surrounded the CO-rich puffs in layer III. These intensely calbindin-immunoreactive neurons were identified as subpopulations of GABA-immunoreactive neurons. Among the most obvious differences in the two monkey species was the distribution of calbindin-positive elements outside of layer III: a dense immunostained matrix surrounded the puffs in layers II, IVB, V, and VI of squirrel monkeys but the immunostained neurons adopted no regular pattern outside layer III in macaques. In addition, although somata lightly immunoreactive for calbindin were present in both species, they were much more abundant in squirrel monkeys than macaques. The pattern of calbindin immunostaining in human area 17 resembled that of macaques in forming an intense matrix that surrounded puffs only in layer III, yet also resembled that of squirrel monkeys by including large numbers of lightly immunoreactive somata. These lightly immunostained somata included a very dense population forming a prominent band in layer IVA of human visual cortex. We conclude that for layer III of primary visual cortex, a similar pattern of neuronal chemistry exists across species of primates which is related to this layer's compartmental organization. Yet for other layers, the expression of calbindin immunoreactivity varies from one species to the next, perhaps reflecting variations in other neuronal properties.

Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey

“…A similar distribution has been observed in the human temporal cortex (del Río and DeFelipe, 1997a). Other authors have reported uneven CB immunostaining in layer III of V1 in the macaque monkey, with the more intense staining observed present around the cytochrome oxidase-rich puffs in layer III (van Brederode et al, 1990;Hendry and Carder, 1993;Blü mcke et al, 1994;Carder et al, 1996). However, in our hands, comparison of alternate sections stained for CB and cytochrome oxidase (unpublished observations) revealed that the distribution of double-bouquet cell axons is unrelated to the pattern of cytochrome oxidase staining in layers II and III, a finding substantiated by Peters and Shetares (1997).…”

Distinctive compartmental organization of human primary visual cortex

“…Future investigations can be expected to reveal additional human specializations of neural organization and function. Candidate specializations include several reported human-monkey differences (56)(57)(58)(59). As the present study illustrates, however (see also ref.…”

Scaling of Inhibitory Interneurons in Areas V1 and V2 of Anthropoid Primates as Revealed by Calcium-Binding Protein Immunohistochemistry

“…Because of the unbiased nature of the stereologic sampling design, these cell counts were not influenced by potential variation in interneuron densities among cytochrome oxidase (CO)-rich blobs, stripes, or non-CO-rich modules [Hendry and Carder, 1993]. Although most interneuron subtypes displayed statistically isometric scaling patterns against total neuron density, CB-ir interneuron subtypes were characterized by a positive allometric scaling relationship.…”