Summary
Immunohistochemistry using antibodies to glutamic acid decarboxylase (GAD) was used to investigate the intralaminar nuclei of the thalamus in rat, cat and monkey. Antibodies to gamma aminobutyric acid (GABA) were also used in the cat. Intralaminar immunoreactive cell bodies were not detected in the rat, but were clearly present in cat and monkey. In the latter species, GABA- or GAD-immunopositive perikarya were distributed throughout the anterior intralaminar nuclei, whereas in the posterior intralaminar complex they prevailed in the lateral part of the centre median nucleus and around the fasciculus retrofiexus. Measurements of the area of immunostained intralaminar cell bodies in cat and monkey indicated that they are represented by small neurons. Experiments in the cat, based on retrograde tracers injections involving large sectors of the frontal and parietal cortices and the head of the caudate nucleus, revealed that the GABA- or GAD-immunoreactive cells and the retrogradely labeled projection neurons represented two separate intralaminar cell populations, although the latter also included small cells. Considerable differences were observed in the immunoreactive GABAergic neuropil of the anterior and posterior intralaminar nuclei. Clusters of densely packed bouton-like immunoreactive elements were detected in the former structures in the rat, cat and monkey, and were especially evident in the central lateral nucleus; immunopositive varicose fibers and puncta were diffusely distributed in the posterior intralaminar structures. Taken together with data from the literature, the present findings indicate that in cat and monkey local circuit inhibitory cells regulate not only the activity of principal thalamic nuclei which project densely upon restricted cortical fields, but also of the intralaminar structures which are widely connected with the cerebral cortex and the striatum. Regional variations in the distribution of GABAergic fibers and terminals suggest major differences in the organization of inhibitory circuits and synaptic arrangements of the anterior and posterior intralaminar thalamus.
Similar content being viewed by others
Abbreviations
- CeM:
-
central medial nucleus
- CL:
-
central lateral nucleus
- CM-Pf:
-
centre median-parafascicular complex
- fr:
-
fasciculus retrofiexus
- Hb:
-
habenular complex
- LD:
-
laterodorsal nucleus
- LP:
-
lateroposterior nucleus
- MD:
-
mediodorsal nucleus
- Pc:
-
paracentral nucleus
- PO:
-
thalamic posterior complex
- PvA:
-
anterior paraventricular nucleus
- Sm:
-
stria medullaris
- VL:
-
ventral lateral nucleus
- VP:
-
ventroposterior complex
References
Balercia G, Bentivoglio M, Ilinsky IA, Kultas-Ilinsky K (1990) Re-evaluation of the ultrastructure of the centre-median nucleus of the rhesus monkey thalamus. Eur J Neurosci Suppl 3:52
Barbaresi P, Spreafico R, Frassoni C, Rustioni A (1986) GABA-ergic neurons are present in the dorsal column nuclei but not in the ventroposterior complex of rats. Brain Res 382:305–326
Bentivoglio M, Minciacchi D, Molinari M, Granato A, Spreafico R, Macchi G (1988) The intrinsic and extrinsic organization of the thalamic intralaminar nuclei. In: Bentivoglio M, Spreafico R (eds) Cellular thalamic mechanisms. Elsevier, Amsterdam, pp 221–237
Clark AS, Schwartz ML, Goldman-Rakic PS (1989) GABA-immunoreactive neurons in the mediodorsal nucleus of the monkey thalamus. J Chem Neuroanat 2:259–267
Fitzpatrick D, Penny GR, Schmechel DE (1984) Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. J Neurosci 7:1809–1829
Gabbott PLA, Somogyi J, Stewart MG, Hamori J (1985) GABA-immunoreactive neurons in the rat dorsal lateral geniculate nucleus: light microscopical observations. Brain Res 346:171–175
Glenn LL, Steriade M (1982) Discharge rate and excitability of cortically projecting intralaminar thalamic neurons during waking and sleep states. J Neurosci 2:1387–1404
Hanker JS, Yates PE, Metz CB, Rustioni A (1977) A new specific sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Histochem J 9:789–792
Harding BN, Powell TPS (1977) An electron microscopic study of the centre-median and ventrolateral nuclei of the thalamus in the monkey. Proc R Soc London B 279:357–412
Harris RM, Hendrickson AE (1987) Local circuit neurons in the rat ventrobasal thalamus: a GABA immunocytochemical study. Neuroscience 21:229–236
Hendrickson AE, Ogren MP, Vaughn JE, Barber RP, Wu JY (1983) Light and electron microscopic immunocytochemical localization of glutamic acid decarboxylase in monkey geniculate complex: evidence for GABAergic neurons and synapses. J Neurosci 3:1245–1262
Houser CR, Vaughn JE, Barber RP, Roberts E (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res 200:341–354
Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580
Hunt CA, Jones EG (1987) Distribution of gamma-aminobutyric neurons and acetylcholinesterase in the monkey intralaminar nuclei. Soc Neurosci Abstr 13:953
Ilinsky IA, Kultas-Ilinsky K (1990) Fine structure of the magnocellular subdivision of the ventral anterior thalamic nucleus (VAmc) of Macaca mulatta. I. Cell types and synaptology. J Comp Neurol 294:455–478
Jayaraman A (1985) Organization of thalamic projections in the nucleus accumbens and the caudate nucleus in cats and its relation with hippocampal and other subcortical afferents. J Comp Neurol 231:396–420
Jones EG (1985) The thalamus. Plenum Press, New York
Jones EG (1989) Defining the thalamic intralaminar nuclei in primates. In: Gainotti G, Bentivoglio M, Bergonzi P, Ferro FM (eds) Neurologia e scienze di base. Vita e Pensiero, Milano, pp 161–193
Kultas-Ilinsky K, Ribak CE, Peterson GM, Oertel WH (1985) A description of the GABAergic neurons and axon terminals in the motor nuclei of the cat thalamus. J Neurosci 5:1346–1369
Ma W, Peschanski M, Ralston III HJ (1987) Fine structure of the spinothalamic projections to the central lateral nucleus of the rat thalamus. Brain Res 414:187–191
Macchi G, Bentivoglio M (1986) The thalamic intralaminar nuclei and the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex, Vol 5. Plenum Press, New York, pp 355–401
Macchi G, Bentivoglio M, Molinari M, Minciacchi D (1984) The thalamo-caudate versus thalamo-cortical projections as studied in the cat with fluorescent retrograde double labeling. Exp Brain Res 54:225–239
Mehler WR (1966) Further notes on the center median nucleus of Luys. In: Purpura DP, Yahrs MD (eds) The thalamus. Columbia University Press, New York, pp 109–122
Montero VM (1986) The interneuronal nature of GABAergic neurons in the lateral geniculate nucleus of the rhesus monkey: a combined HRP and GABA-immunocytochemical study. Exp Brain Res 64:615–622
Montero VM (1989) The GABA-immunoreactive neurons in the interlaminar regions of the cat lateral geniculate nucleus: light and electron microscopic observations. Exp Brain Res 75:497–512
Montero VM, Zempel J (1985) Evidence for two types of GABA-containing interneurons in the A-laminae of the cat lateral geniculate nucleus: a double-label HRP and GABA-immunohistochemical study. Exp Brain Res 60:603–609
Mugnaini E, Dahl AL (1983) Zinc-aldehyde fixation for light microscopic immunocytochemistry of nervous tissues. J Histochem Cytochem 31:1435–1438
Norita M, Katoh Y (1987) The GABAergic neurons and axon terminals in the lateralis medialis-suprageniculate nuclear complex of the cat: GABA-immunocytochemical and WGA-HRP studies by light and electron microscopy. J Comp Neurol 263:54–67
Oertel WH, Schmechel DE, Tappaz ML, Kopin IJ (1981) Production of a specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience 6:2689–2700
Ohara PT, Lieberman AR, Hunt SP, Wu J-Y (1983) Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat: immunohistochemical studies by light and electron microscopy. Neuroscience 8:189–211
Ottersen OP, Storm-Mathisen J (1984) GABA-containing neurons in the thalamus and pretectum of the rodent: an immunocytochemical study. Anat Embryol 170:197–207
Penney JB, Young AB (1981) GABA as the pallidothalamic neurotransmitter: implications for basal ganglia function. Brain Res 207:195–199
Penny GR, Itoh K, Diamond IT (1982) Cells of different sizes in the ventral nuclei project to different layers of the somatic cortex in the cat. Brain Res 242:55–65
Penny GR, Fitzpatrick D, Schmechel DE, Diamond IT (1983) Glutamic acid decarboxylase-immunoreactive neurons and horseradish peroxidase labeled projection neurons in the ventral posterior nucleus of the cat and Galago senegalensis. J Neurosci 3:1868–1887
Penny GR, Conley M, Schmechel DE, Diamond IT (1984) The distribution of glutamic acid decarboxylase immunoreactivity in the diencephalon of the opossum and rabbit. J Comp Neurol 228:38–56
Rausell E, Avendano C (1985) Thalamocortical neurons projecting to superficial and deep layers in parietal, frontal and prefrontal regions in the cat. Brain Res 347:159–165
Rinvik E, Ottersen OP, Storm-Mathisen J (1987) Gamma-aminobutyrate-like immunoreactivity in the thalamus of the cat. Neuroscience 21:781–805
Scheibel ME, Scheibel AB (1966) The organization of the nucleus reticularis thalami: a Golgi study. Brain Res 1:43–62
Scheibel ME, Scheibel AB (1967) Structural organization of nonspecific thalamic nuclei and their projection toward cortex. Brain Res 6:60–94
Smith Y, Parent A (1986) Differential connections of caudate nucleus and putamen in the squirrel monkey (Saimiri sciureus). Neuroscience 18:347–371
Smith Y, Seguela P, Parent A (1987) Distribution of GABA-immunoreactive neurons in the thalamus of the squirrel monkey (Saimiri sciureus). Neuroscience 22:579–591
Spreafico R, Schmechel DE, Ellis LC, Rustioni A (1983) Cortical relay neurons and interneurons in the n. ventralis posterolateralis of cats: a horseradish peroxidase, electron microscopic, Golgi and immunocytochemical study. Neuroscience 9:491–509
Steriade M, Llinas RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649–742
Steriade M, Parent A, Hada J (1984) Thalamic projections of nucleus reticularis thalami of cat: a study using retrograde transport of horseradish peroxidase and double fluorescent tracers. J Comp Neurol 229:531–547
Steriade M, Deschênes M, Domich L, Mulle C (1985) Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. J Neurophysiol 54:1473–1497
Sternberger LA (1979) Immunocytochemistry. John Wiley & Sons, New York
Tömböl T, Bentivoglio M, Macchi G (1990) Neuronal cell types in the thalamic intralaminar central lateral nucleus of the cat. Exp Brain Res 81:491–499
Tseng G-F, Royce GJ (1986) A Golgi and ultrastructural analysis of the centromedian nucleus of the cat. J Comp Neurol 245:359–378
Weinberg RJ, Bentivoglio M, Phend K, Schmechel DE, Rustioni A (1985) A new double-labeling method demonstrates transmitter-specific projections. Neurosci Lett 55:349–353
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bentivoglio, M., Spreafico, R., Minciacchi, D. et al. GABAergic interneurons and neuropil of the intralaminar thalamus: an immunohistochemical study in the rat and the cat, with notes in the monkey. Exp Brain Res 87, 85–95 (1991). https://doi.org/10.1007/BF00228509
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00228509