The distribution of calbindin, calretinin and parvalbumin immunoreactivity in the human thalamus
Introduction
The calcium-binding proteins calbindin-D28k (calbindin), calretinin and parvalbumin belong to the EF-hand family of calcium-binding proteins (for reviews see Persechini et al., 1989, Heizmann and Hunziker, 1991, Baimbridge et al., 1992, Andressen et al., 1993). These proteins have been implicated in the buffering (Fierro and Llano, 1996, McMahon et al., 1998) and transport of calcium as well as in the regulation of various enzyme systems (Heizmann, 1992). Although, in the cerebral cortex and hippocampus, the calcium-binding proteins are expressed in a large proportion of GABA-ergic cells, they are also variously associated with other neurotransmitters; e.g. parvalbumin is found in cells containing glycine and glutamate as well (for review see Baimbridge et al., 1992). Also, parvalbumin is often associated with fast-firing neurones (Kawaguchi et al., 1987) but, as yet, there is no such physiological specificity associated with calbindin or calretinin containing neurones.
Although the exact function of the calcium-binding proteins is unknown, these proteins are present in distinct subpopulations of neurones thus making them very useful anatomical markers for identifying specific subgroups of neurones (Andressen et al., 1993). Numerous studies of the mammalian brain (Jones and Hendry, 1989, Celio, 1990, Jacobowitz and Winsky, 1991, Resibois and Rogers, 1992, Rogers and Resibois, 1992, Winsky et al., 1992, Arai et al., 1994, De Biasi et al., 1994, Molinari et al., 1994, Gutierrez et al., 1995) have shown that the calcium-binding proteins are distributed in a heterogeneous fashion and that they are very useful for delineating nuclear boundaries which are difficult to distinguish on cytoarchitectural criteria alone. In particular, previous studies on the monkey thalamus investigating the distribution of calbindin and parvalbumin (Jones and Hendry, 1989) and calretinin (Fortin et al., 1996) have shown the advantage of using the localisation of the calcium-binding proteins to assist in the delineation of thalamic nuclear subdivisions. Furthermore, Jones (1998) has suggested that the distribution of calbindin and parvalbumin immunoreactivity in the thalamus provides a very useful indicator for the identification of different anatomical and functional types of thalamocortical projection neurones. Based on studies in the monkey thalamus, Jones (1998) proposes that calbindin immunoreactive cells distributed throughout the thalamus provide a matrix of neurones which project diffusely to superficial layers of the cortex and are involved in multiple aspects of sensory experience essential for consciousness; by contrast, parvalbumin immunoreactive neurones are localised only in specific thalamic nuclei and form a core of neurones which project in a highly ordered fashion to middle layers of the cortex and are involved in perception. Thus, a detailed study of the regional and cellular distribution of the calcium-binding proteins in the human thalamus may provide a basis for a better understanding of the anatomical and functional organisation of the thalamus in the human brain.
Previous studies on the distribution of the calcium-binding proteins in the human thalamus have been either very generalised studies directed at establishing a stereotactic atlas (Morel et al., 1997), or have focused on one thalamic nuclear group (Münkle et al., 1999) or the distribution of one calcium-binding protein (Fortin et al., 1998). In the present study a very detailed study of the regional and cellular localisation of all three calcium-binding proteins — calbindin, calretinin and parvalbumin — throughout the full extent of the human thalamus has been undertaken in order to gain a better understanding of the anatomical and functional complexities of the primate thalamus.
Section snippets
Materials and methods
The human brain tissue was obtained from the New Zealand Neurological Foundation Human Brain Bank and the study was approved by the University of Auckland Human Subjects Ethics Committee. Tissue was obtained from eight post-mortem brains of cases with no known history of neurological disease (see Table 1); the average age of the eight cases was 58.5 years and the average post-mortem delay was 13 h. The brains were perfusion fixed via the internal carotid and basilar arteries using 0.1 M
Results
The results are presented in two parts. First, a detailed description is provided of the regional and cellular localisation of the calcium-binding proteins in each of the component nuclei of the major nuclear groups in the human thalamus. This description is based on the findings in Fig. 1, Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8, Fig. 9, Fig. 10, Fig. 11. Fig. 1, Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8 are low power photomicrographs which show the regional nuclear
Discussion
This is the first major study on the detailed distribution of the three calcium-binding proteins — calbindin, calretinin and parvalbumin — in the human thalamus. The major finding in this study is the demonstration that the calcium-binding proteins, especially calbindin and parvalbumin, generally show a complementary staining pattern in many nuclear complexes of the human thalamus. The third calcium-binding protein — calretinin — shows a more restricted distribution in the human thalamus and
Acknowledgements
This study was supported by grants from the Health Research Council of New Zealand, the New Zealand Neurological Foundation, the New Zealand Lottery Board and the University of Auckland Research Committee. M.C.M. was supported by a scholarship from the German Academic Exchange Service (Doktorandenstipendium HSPIII).
References (39)
- et al.
Distribution of calretinin, calbindin-D28k, and parvalbumin in the rat thalamus
Brain Res. Bull.
(1994) - et al.
Calcium-binding proteins in the nervous system
Trends Neurosci.
(1992) Calbindin-D28k and parvalbumin in the rat nervous system
Neuroscience
(1990)- et al.
Calretinin immunoreactivity in the thalamus of the squirrel monkey
J. Chem. Neuroanat.
(1996) - et al.
Calretinin-immunoreactive neurons in the human thalamus
Neuroscience
(1998) - et al.
Intracellular calcium-binding proteins: more sites than insights
Trends Biochem. Sci.
(1991) - et al.
Calretinin-immunoreactive neocortical interneurons are unaffected in Alzheimer’s disease
Neurosci. Lett.
(1993) Viewpoint: the core and matrix of thalamic organization
Neuroscience
(1998)- et al.
Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin
Brain Res.
(1987) - et al.
Colocalization of parvalbumin, calretinin and calbindin D-28k in human cortical and subcortical visual structures
J. Chem. Neuroanat.
(1997)
Calbindin-D28k buffers intracellular calcium and promotes resistance to degeneration in PC12 cells
Mol. Brain Res.
New views of the thalamic reticular nucleus in the adult and the developing brain
Trends Neurosci.
Calcium-binding protein immunoreactivity delineates the intralaminar nuclei of the thalamus in the human brain
Neuroscience
The EF-hand family of calcium-modulated proteins
Trends Neurosci.
Calretinin and calbindin-D28k in rat brain: patterns of partial co-localization
Neuroscience
The role of the thalamus in functional neurosurgery
Neurosurg. Clin. N. Am.
The morphological and chemical characteristics of striatal neurons immunoreactive for the alpha1-subunit of the GABA(a) receptor in the rat
Neuroscience
Calretinin distribution in the thalamus of the rat: immunohistochemical and in situ hybridization histochemical analyses
Neuroscience
Calcium-binding proteins: selective markers of nerve cells
Cell Tissue Res.
Cited by (90)
Mesocircuit mechanisms in the diagnosis and treatment of disorders of consciousness
2023, Presse MedicaleAdaptively navigating affordance landscapes: How interactions between the superior colliculus and thalamus coordinate complex, adaptive behaviour
2022, Neuroscience and Biobehavioral ReviewsNeural correlates of consciousness and related disorders: From phenotypic descriptors of behavioral and relative consciousness to cortico-subcortical circuitry
2022, NeurochirurgieCitation Excerpt :The nuclei have been placed in specific groups directly involved in sensory-motor activity, unspecific groups [57,58], or in principal or relay (=sensorimotor), limbic (anterior, midline, and medial intralaminar nuclei) and connection nuclei groups between the relay and the limbic groups [59]. According to the calbindin and parvalbumin bindings of cells, nuclei have also been segregated into matrix-calbindin and core-parvalbumin groups, which involve the main parts of the central lateral and the parafascicular nuclei, and the centromedian and the reticular nuclei respectively [60,61]. The notion of central thalamus was highlighted by Schiff [62] and covers the extended central region of the thalamus centered on the intralaminar nuclei and the close neighborhood.
The thalamus integrates the macrosystems of the brain to facilitate complex, adaptive brain network dynamics
2021, Progress in NeurobiologyCore and matrix thalamic sub-populations relate to spatio-temporal cortical connectivity gradients
2020, NeuroImageCitation Excerpt :We denote this measure CPT: positive levels reflect voxels with higher CALB1 levels, negative levels reflect voxels with higher PVALB levels and values of zero denote a balance between the two populations. To validate the measure, the mean CPT value was calculated for each of 31 pre-defined thalamic sub-nuclei that fell into 6 distinct groups (Table 1) and compared quantitatively to results obtained from direct histological (Münkle et al., 2000) and immunohistochemistry (Arai et al., 1994) analyses (data were extracted from tables within each of the referenced documents). We observed a positive correlation between these direct measurements and our gene-expression based proxy, CPT (r = 0.546; p = 0.003; Fig. S1).