Delineation of thalamic nuclei immunoreactive for calcium-binding proteins in and around the posterior pole of the ventral posterior complex
Introduction
The discovery of the differential expression of the calcium-binding proteins, calbindin and parvalbumin, in relay neurons of the primate thalamus (Jones and Hendry, 1989) has led to a number of lines of investigation in which these specific expression patterns have been exploited for different ends. In one case, recognition that calbindin-immunoreactive cells project rather diffusely to superficial layers of the cerebral cortex, while parvalbumin-immunoreactive cells project in an areal- and topographically-constrained fashion to middle layers (Rausell and Jones, 1991a, Rausell et al., 1992, Diamond et al., 1993, Jones, 1998a) has resulted in a new view of thalamocortical organization, based on a diffusely organized matrix of calbindin cells extending throughout the thalamus and precisely organized sets of parvalbumin cells, each forming a core to the principal relay nuclei (Jones, 1998b, Jones, 1998c, Jones, 2001b).
In other cases, the differential distributions of neurons immunostained for calbindin or parvalbumin have been used to provide new delineations of nuclear complexes such as the pulvinar (Gray et al., 1999, Gutierrez et al., 2000). In a further example of this approach, a localized concentration of calbindin-immunoreactive fiber ramifications in the ventral posterior part of the thalamus has been postulated to delineate a region of thalamus that forms the specific relay for pain and noxious thermal messages to regions of cerebral cortex in the vicinity of the insula (Craig et al., 1994, Blomquist et al., 2000). Called as VMpo by its protagonists, the relevant region has been difficult to relate to existing architectonic or chemoarchitectonic parcellations of the caudal thalamus, mainly for lack of detail and a lack of correlation with pre-existing data. An atlas of sections immunostained for three calcium-binding proteins or histochemically stained for cytochrome oxidase is now presented in an effort to pinpoint the relevant region in relation to the conventional architecture and terminology of this part of the monkey caudal thalamus. Most of what is described here, based on other sectioned monkey brains, has been published in previous accounts (Rausell and Jones, 1991a, Rausell et al., 1992, Steriade et al., 1997, Jones, 1998a) and a preliminary account of the present material has appeared (Chan and Jones, 1999). The complete atlas will be published in greater detail elsewhere. The nomenclature is the same as that used in the earlier papers, which derives from that of Olszewski (1952), Jones (1985) and Hirai and Jones (1989).
The atlas is derived from a single, serially sectioned brain from a 4-year-old male Macaca mulatta monkey. The animal was deeply anesthetized and perfused through the heart with normal saline followed by 4% paraformaldehyde in 0.1 M phosphate buffer (pH 7.4). The diencephalon was blocked in the frontal Horsley–Clark plane, post-fixed overnight in the same fixative, cryoprotected in 30% sucrose, frozen in dry ice, and serially sectioned in the frontal plane at 30 μm on a sliding microtome. Sections were collected in serial order through the full antero-posterior extent of the thalamus. Every sixth section was mounted on glass slides, lipid extracted and stained with thionin. The intervening sections were stained, free floating, for cytochrome oxidase, for myelin, or immunocytochemically for 28 kDa calbindin, 29 kDa calretinin or parvalbumin. In this way, six alternating series of sections stained for each marker, each section at 180 μm intervals, were built up.
For immunostaining, the following polyclonal antisera or monoclonal antibodies were used: for parvalbumin, a sheep antiparvalbumin antiserum (Jones and Hendry, 1989) or a mouse monoclonal antibody (Sigma); for 28 kDa calbindin, a rabbit anticalbindin antiserum that also recognizes 29 kDa calretinin (Jones and Hendry, 1989, Rogers, 1987), or a mouse monoclonal antibody specific for calbindin (Sigma); for calretinin a rabbit anticalretinin antiserum (Chemicon). The monoclonal antibodies and antisera were diluted in 0.1 M phosphate buffer containing 0–25% Triton X-100 and 3% normal serum from the species in which the secondary antibodies to be used was raised. Final dilutions of the primary antibodies were 1:3000 or 1:2000 (for calretinin, only). Sections were preincubated for 1–2 h in 0.1 M phosphate buffer containing 0.25% Triton X-100 and 3% normal serum before being transferred to the primary antibody-containing solution for 12–24 h at 4 °C. After washing, sections were transferred to secondary IgG solutions for 1 h, reincubated in avidin–biotin–peroxidase (ABC) complex and bound antibodies revealed by incubation in 0.02% 3,3′ diaminobenzidine, HCl and 0.001% hydrogen peroxide.
A series of sections from the thalami of many other M. mulatta brains, stained by the same procedures were available for comparison. In one specific case, alternate 30 μm thick frozen sections through the thalamus were immunostained for calbindin using the rabbit anticalbindin antiserum or the commercial mouse monoclonal antibody to calbindin.
Section snippets
Results
Examining the series of alternately stained sections in posterior to anterior order (Fig. 1, Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8), the posterior nuclear region of the thalamus can be distinguished as a region of predominantly weak CO staining that is traversed by the (unstained) fiber bundles of the corticotectal tract and associated fiber systems. Here and there, within it are patches of denser CO staining that represent the islands of neurons belonging to the
Discussion
This systematic analysis of calbindin and parvalbumin immunoreactivity in relation to histochemical staining of the nuclear landmarks in the posterior region of the monkey thalamus reveals no new pattern of localization and, thus, the earlier descriptions require no modification (Rausell and Jones, 1991a, Rausell et al., 1992, Jones, 1998a). The principal point at issue in undertaking this study, the identification of an isolated focus of calbindin-rich fiber terminations, called by Craig et
Acknowledgements
Supported by Grant number NS 21377 from the National Institutes of Health, United States Public Health Service.
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