Two types of interneuron in the dorsal lateral geniculate nucleus of the rat: A combined NADPH diaphorase histochemical and GABA immunocytochemical study

Abstract

The rationale for this study was to provide a comprehensive light microscopical description of the morphology of diaphorase-reactive neurons and neuropil elements in the dorsal lateral geniculate nucleus (dLGN) of the rat. An additional objective was to quantitatively assess whether a subpopulation of the diaphorase-reactive neurons, previously shown to be GABA-immunoreactive, constitute a distinct type of local-circuit neuron in the rat dLGN. Diaphorase activity was localised in a population of predominantly bipolar fusiform neurons. These cells were weak to moderately stained and possessed the morphological features of intrinsic inhibitory neurons, previously called class B neurons in the rat dLGN. Quantitative estimates indicated that the diaphorase-reactive neurons constituted approximately 10% of the total neuron composition of the dLGN. The majority (about 83%) of the diaphorase-reactive cells were located in the lateral half of the nucleus. In addition, a dense plexus of diaphorase-reactive varicose fibres was found throughout the dLGN lying between the oriented fibre bundles coursing dorsoventrally through the LGN. Diaphorase-reactive punctae were found to be closely associated with the somata and proximal dendritic segments of nonreactive neurons and also with the stained proximal dendritic segments of diaphorase-reactive dLGN neurons. The source of the diaphorase-reactive fibres in the dLGN was unknown. Evidence suggests, however, that they are of extrinsic origin. The GABA-immunoreactive nature of the diaphorase neurons in the dLGN was demonstrated by colocalising GABA immunoreactivity within the somata of diaphorase-reactive cells. The majority (> 90%) of diaphorase-reactive dLGN neurons were GABA-immunopositive. Also present was a distinct population of GABA-immunopositive neurons that were not diaphorase-reactive. In this study, cells that were solely GABA-immunopositive have been called class B1 neurons, while cells that were both diaphorase-reactive and GABA-immunoreactive have been called class B2 neurons. Size-frequency distributions of somatic profile areas established that the two populations of GABA-immunoreactive neuron were significantly different. Class B1 neurons constituted 57%, with class B2 cells representing 43% of all GABA-immunostained neurons in the rat dLGN. The characteristic morphological features, neurochemical identity and frequency of the diaphorase-reactive neurons in the rat dLGN indicate that they represent a subpopulation of inhibitory interneurons with the ability to affect intrinsic dLGN operations and thalamocortical interactions using the neuromodulator nitric oxide.

Nitric oxide synthase in the adult and developing thalamus: Histochemical and immunohistochemical study in the rat

“…Outside the midline nuclei, the only thalamic site containing a relatively high number of neurons that express NOS was LG, a notable exception to the otherwise striking lack of positive cell bodies in the primary thalamic relay nuclei. The present data on the distribution of NADPH-d-positive neurons in LG are in agreement with previous studies in the adult rat (Mitrofanis, 1992;Vincent and Kimura, 1992;Gabbott and Bacon, 1994).…”

“…As for the thalamic cell types that were found in the present study to express NOS, it has been reported that a large proportion of NADPH-d-positive cell bodies in the rat DLG are GABA-immunoreactive and represent a subpopulation of interneurons (Mitrofanis, 1992;Gabbott and Bacon, 1994). In support of the concept that subsets of thalamic interneurons may express NOS, this enzyme has also been detected in a subpopulation of GABAergic cells in the cat VB (Meng et al, 1996).…”

A classification of NOergic neurons in the inferior colliculus of rat according to co-existence with classical amino acid transmitters

“…Recently several investigators have described the distribution of NOergic neurons in relation to aminergic neurons in different regions of the central nervous system, including the zona inserta 17) , prefrontal cortex 13) , medulla oblongata 21) , hippocampus 37) , cuneate nucleus 35) , olfactory bulb 1) , lateral geniculate nucleus 14) , spinal cord 31) , and cerebral cortex 36) . Nevertheless, little is known about the relationship between NO and neuroactive amino acids in the auditory nuclei.…”

“…Indeed, the above approach has been used widely for mapping NOS-containing (presumably NOergic) neurons in the central nervous system 3,38) . NADPH-d histochemistry has also been combined with immunohistochemistry to assess relationships between the distribu-tion of NO and traditional neurotransmitters in various regions of the CNS 1,14,30,35,37) . Several studies suggest that NO and NOS play a role in audition.…”

Two types of interneurons in the cat visual thalamus are distinguished by morphology, synaptic connections, and nitric oxide synthase content

“…Electron microscopic data showed that these neurons were a source of GABAergic terminals within the ventrobasal nucleus (Meng et al, 1997). Similarly, a subset of interneurons in the rat LGN have been identified using by using nicotinadamine phosphate (NADPH)-diaphorase histochemistry to stain for BNOS (Gabbot and Bacon, 1994).…”