DOI: 10.1111/j.1460-9568.1989.tb00791.x. Differential Calcium Binding Protein Immunoreactivity Distinguishes Classes of Relay Neurons in Monkey Thalamic Nuclei

Differential Calcium Binding Protein Immunoreactivity Distinguishes Classes of Relay Neurons in Monkey Thalamic Nuclei

10.1111/j.1460-9568.1989.tb00791.x

Crossref journal-article

Wiley

European Journal of Neuroscience (311)

Abstract

AbstractThe distributions of neurons displaying immunoreactivity for two calcium binding proteins, parvalbumin and 28Kd calbindin, were studied in the thalamus of M. fascicularis. Colocalization experiments were carried out to determine the extent to which parvalbumin‐ and calbindin‐like immunoreactivity was found in the same cells and the extent to which either was localized in GABAergic interneurons. Anterograde and retrograde tracing experiments involving the fluorescent tracer, fast blue, were also used to determine that cells expressing the calcium binding proteins projected upon the cerebral cortex.In the dorsal thalamus, nuclei are distinguished by different patterns of parvalbumin‐like and calbindin‐like immunoreactivity. In certain nuclei, for example the lateral dorsal and anterior pulvinar, neurons express immunoreactivity for only one of the calcium binding proteins. In others, neurons in different layers, for example the dorsal lateral geniculate nucleus, or in different compartments, for example the intralaminar nuclei, express immunoreactivity for either parvalbumin or calbindin; in other nuclei, for example the ventral group, neurons are mixed and immunoreactivity for parvalbumin and calbindin is commonly colocalized. In the ventral thalamus and epithalamus, similar patterns are observed.Colocalization of parvalbumin‐ and GABA‐immunoreactivity is found in all cells of the reticular nucleus but only in certain cells in selected nuclei of the dorsal thalamus, namely the dorsal lateral geniculate and magnocellular medial geniculate. No calbindin‐positive cells are also GABA‐positive.Most parvalbumin and/or calbindin positive cells in the dorsal thalamus project to the cerebral cortex, as indicated by the retrograde tracing studies, and many parvalbumin positive fibres entering the cerebral cortex could also be shown to contain fast blue anterogradely transported from a thalamic injection.Most of the major sensory and motor pathways entering the dorsal thalamus express parvalbumin immunoreactivity. The optic tract also expresses calbindin immunoreactivity but most other calbindin positive fibres entering the thalamus ascend in the midbrain tegmentum.The differential distributions of parvalbumin and calbindin implied by these results suggest that thalamic cells belonging to different functional systems and projecting differentially upon the cerebral cortex can be distinguished by differential expression of these or closely related calcium binding proteins. This may yield clues to their differential responsivity to afferent driving.

Bibliography

Jones, E. G., & Hendry, S. H. C. (1989). Differential Calcium Binding Protein Immunoreactivity Distinguishes Classes of Relay Neurons in Monkey Thalamic Nuclei. European Journal of Neuroscience, 1(3), 222â246. Portico.

Authors 2

E. G. Jones (first)
S. H. C. Hendry (additional)

References 82 Referenced 334

10.1113/jphysiol.1964.sp007493
10.1016/0006-8993(82)90804-6
10.1016/0006-8993(84)90624-3
10.1016/0006-8993(82)90526-1
10.1016/0006-8993(68)90100-5
{'key': 'e_1_2_2_7_1', 'first-page': '337', 'volume-title': 'Somatosensory Integration in the Thalamus', 'author': 'Bentivoglio M.', 'year': '1983'} / Somatosensory Integration in the Thalamus by Bentivoglio M. (1983)
10.1073/pnas.82.5.1414
10.1002/cne.901180106
10.1007/BF00217563
10.1126/science.3945815
10.1038/293300a0
10.1038/323715a0
10.1113/jphysiol.1971.sp009581
10.1016/0006-8993(75)90553-3
10.1523/JNEUROSCI.08-03-00988.1988 / J. Neurosci. / Heterogeneity of GABAergic cells in cat visual cortex by Demeulemeester H. (1988)
10.1152/jn.1984.51.6.1196
10.1016/0304-3940(85)90590-7
10.1210/endo-112-1-290
10.1523/JNEUROSCI.03-04-00673.1983
10.1016/0006-8993(84)90512-2
10.1073/pnas.82.24.8780
10.1007/BF01731373
10.1007/BF01946439
10.1073/pnas.79.23.7243
10.1016/0143-4160(87)90034-0
10.1002/cne.901820108
{'key': 'e_1_2_2_28_1', 'article-title': 'Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities', 'author': 'Hendry S. H. C.', 'year': '1988', 'journal-title': 'Exp. Brain Res.'} / Exp. Brain Res. / Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities by Hendry S. H. C. (1988)
10.1152/jn.1972.35.4.518 / J. Neurophysiol. / Relay of receptive‐field properties in dorsal lateral geniculate nucleus of the cat by Hoffman K.‐P. (1972)
10.1007/BF01181527
10.1523/JNEUROSCI.07-11-03378.1987 / J. Neurosci. / Segregation of form, color and stereopsis in primate area 18 by Hubel D. H. (1987)
10.1002/cne.901460402
10.1098/rspb.1977.0085
10.1073/pnas.83.20.7578
10.1113/jphysiol.1984.sp015154
10.1113/jphysiol.1984.sp015153
10.1038/294765a0
10.1007/BF00592574
{'key': 'e_1_2_2_39_1', 'first-page': '521', 'volume-title': 'Cerebral Cortex, Vol. 1, Cellular Components of the Cerebral Cortex', 'author': 'Jones E. G.', 'year': '1984'} / Cerebral Cortex, Vol. 1, Cellular Components of the Cerebral Cortex by Jones E. G. (1984)
10.1007/978-1-4615-1749-8
10.1007/BF00238863
{'key': 'e_1_2_2_42_1', 'first-page': '780', 'article-title': 'Two classes of cortical GABA neurons defined by differential calcium binding protein and parvalbumin immunoreactivity', 'volume': '14', 'author': 'Jones E. G.', 'year': '1988', 'journal-title': 'Neurosci. Abstr.'} / Neurosci. Abstr. / Two classes of cortical GABA neurons defined by differential calcium binding protein and parvalbumin immunoreactivity by Jones E. G. (1988)
10.1002/cne.901540402
10.1007/BF00236848
10.1016/0006-8993(78)90464-X
10.1016/0006-8993(87)90921-8
10.1146/annurev.bi.49.070180.002421
10.1016/S0065-3233(08)60470-2
10.1016/0006-8993(87)90575-0
10.3109/10409238009105467
10.1007/BF00238305
10.1016/0006-8993(76)90002-0
10.1523/JNEUROSCI.07-11-03371.1987 / J. Neurosci. / Connections between layer 4B of area 17 and thick cytochrome oxidase strips of area 18 in the squirrel monkey by Livingstone M. S. (1987)
10.1007/BF00236222
{'key': 'e_1_2_2_55_1', 'first-page': '3', 'volume-title': 'Somatosensory Integration in the Thalamus', 'author': 'Macchi G.', 'year': '1983'} / Somatosensory Integration in the Thalamus by Macchi G. (1983)
10.1007/978-1-4613-2149-1_10
10.1007/BF00493380
10.1152/jn.1985.54.4.782
10.1152/physrev.1982.62.1.1
10.1210/edrv-3-4-331
10.1523/JNEUROSCI.03-09-01868.1983 / J.Neurosci. / Glutamic acid decarboxylase immunoreactive neurons and horseradish peroxidase labeled projection neurons in the ventral posterior nucleus of the cat and Galago senegalensis by Penny G. R. (1983)
10.1093/brain/79.2.364
10.1007/BF00222366
10.1083/jcb.105.3.1343
{'key': 'e_1_2_2_65_1', 'first-page': '81', 'volume-title': 'Cerebral Cortex, Vol. 3, Visual Cortex', 'author': 'Rosenquist A. C.', 'year': '1985'} / Cerebral Cortex, Vol. 3, Visual Cortex by Rosenquist A. C. (1985)
10.1016/0304-3940(85)90221-6
{'key': 'e_1_2_2_67_1', 'article-title': 'Expression of the parvalbumin gene in the rat brain: a study using hybridization histochemistry', 'author': 'Seto‐Ohshima A.', 'year': '1988', 'journal-title': 'Brain Res.'} / Brain Res. / Expression of the parvalbumin gene in the rat brain: a study using hybridization histochemistry by Seto‐Ohshima A. (1988)
{'key': 'e_1_2_2_68_1', 'volume-title': 'Circuitry and State Dependent Functions of the Thalamus', 'author': 'Steriade M.', 'year': '1989'} / Circuitry and State Dependent Functions of the Thalamus by Steriade M. (1989)
10.1002/cne.902680104
10.1002/cne.902620409
10.1152/jn.1974.37.4.722 / J. Neurophysiol. / Properties of cat retinal ganglion cells: a comparison of W‐cells with X‐ and Y‐cells by Stone J. (1974)
10.1038/301517a0
10.1152/jn.1982.47.5.869
10.1523/JNEUROSCI.07-06-01843.1987 / J. Neurosci. / CaBP immunoreactivity labels the terminal field of nucleus laminaris of the barn owl by Takahashi T. (1987)
10.1016/0165-3806(86)90098-2
10.1016/0003-9861(74)90239-2
{'key': 'e_1_2_2_77_1', 'first-page': '32', 'article-title': 'Thalamusstudien I‐III', 'volume': '50', 'author': 'Vogt C.', 'year': '1941', 'journal-title': 'J.Psychol. Neurol.'} / J.Psychol. Neurol. / Thalamusstudien I‐III by Vogt C. (1941)
10.1016/B978-0-12-171402-4.50012-5
10.1126/science.152.3723.791
10.1002/cne.902130203
10.1016/0006-8993(75)90333-9
10.1016/0006-8993(79)90728-5
10.1016/0361-9230(81)90004-6

Dates

Type	When
Created	19 years, 4 months ago (April 7, 2006, 7:56 p.m.)
Deposited	1 year, 10 months ago (Oct. 22, 2023, 12:39 a.m.)
Indexed	1 week, 5 days ago (Aug. 23, 2025, 9:26 p.m.)
Issued	36 years, 4 months ago (May 1, 1989)
Published	36 years, 4 months ago (May 1, 1989)
Published Online	19 years, 4 months ago (April 7, 2006)
Published Print	36 years, 4 months ago (May 1, 1989)

Funders 0

None

BibTeX

@article{Jones_1989, title={Differential Calcium Binding Protein Immunoreactivity Distinguishes Classes of Relay Neurons in Monkey Thalamic Nuclei}, volume={1}, ISSN={1460-9568}, url={http://dx.doi.org/10.1111/j.1460-9568.1989.tb00791.x}, DOI={10.1111/j.1460-9568.1989.tb00791.x}, number={3}, journal={European Journal of Neuroscience}, publisher={Wiley}, author={Jones, E. G. and Hendry, S. H. C.}, year={1989}, month=may, pages={222–246} }

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