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Expression of AMPA-Selective Glutamate Receptor Subunits in Morphologically Defined Neurons of the Mammalian Cochlear Nucleus

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Expression of AMPA-Selective Glutamate Receptor Subunits in Morphologically Defined Neurons of the Mammalian Cochlear Nucleus The Journal of Neuroscience, May 1993, 73(5): 1932-l 946 Expression of AMPA-Selective Glutamate Receptor Subunits in Morphologically Defined Neurons of the Mammalian Cochlear Nucleus Chyren Hunter, Ronald S. Petralia, Thuc Vu, and Robert J. Wenthold Section on Neurotransmitter Receptor Biology, Laboratory of Neurochemistry, NIDCD, National Institutes of Health, Bethesda, Maryland 20892 Glutamate and related amino acids mediate fast excitatory [Key words: glutamate receptor, in situ hybridization, neurotransmission in the vertebrate CNS via ligand-gated cochlear nucleus, rat, auditory system, cell-specific mRNA] cationic channels in the neuronal membrane. These chan- nels are composed of different subunits that assemble into All sound information detected by sensorycells in the inner ear a functional receptor/channel complex. Although studies is transmitted through the auditory nerve to the cochlear nucleus have shown that these subunits are differentially expressed (CN). Neurons receiving auditory nerve input are present in neurons, few studies have quantitatively addressed the throughout the CN and have been thoroughly studied morpho- cell-specific expression of glutamate subunits in relation to logically and physiologically. At least five morphologically dis- known glutamatergic pathways. In the vertebrate auditory tinct neurons receive input from the auditory nerve; they are system, glutamate is the proposed neurotransmitter of the concentrated in different regions of the CN and include the auditory nerve and parallel fiber pathways. In situ hybridiza- spherical, globular, stellate, octopus, and fusiform neurons. The tion histochemistry was used to localize AMPA-selective type of synaptic contact made with the auditory nerve differs glutamate receptor subunit mRNAs in seven cell types of among cell types, ranging from nearly entirely axosomatic for the rat cochlear nucleus. GIuRl -GIuR4 AMPA-selective sub- sphericalceils to entirely dendritic for fusiform cells (seereview units were all expressed in cochlear nucleus neurons; how- by Cant and Morest, 1984). Physiological responsesto sound ever, the subunits expressed in identified cells varied with are distinct for each cell type, and each cell type has a charac- the cell type. Granule cells, previously not known to receive teristic projection pattern to other nuclei in the brain. Spherical glutamatergic input, expressed GluRP and GIuR4 subunits. bushy cells of the rostra1 anteroventral CN (AVCN) project Cartwheel and stellate interneurons in the dorsal cochlear bilaterally to the medial superior olives and to the ipsilateral nucleus, which receive parallel fiber input, expressed all four lateral superior olive in the brainstem (Cant, 1981). The evoked subunits. Neurons receiving synaptic input from the auditory responsesof theseneurons are “primary-like,” thus resembling nerve, including globular, round, spherical, and fusiform cells, input from the auditory nerve (Rhode et al., 1983; Caspary, expressed GIuR2, GIuR3, and GIuR4 subunits. Furthermore, 1986). “Notch-primary-like” and “primary-like” responsesare a subpopulation of round cells in the ventral cochlear nu- characteristic of globular cells (Rhode et al., 1983; Caspary, cleus, and fusiform cells in the dorsal cochlear nucleus, ex- 1986) and these cells send projections to the ipsilateral lateral pressed the GluR3 subunit at greatly reduced levels com- nucleusof the trapezoid body and the contralateral medial nu- pared to neighboring cells. The results confirm the auditory cleus of the trapezoid body (Tolbert and Morest, 1982; seere- nerve and parallel fiber pathways as glutamatergic and iden- view by Cant, 199 1). Octopus and stellate neurons show re- tify a third synaptic population, projecting to granule cells, sponse patterns that do not resemble auditory nerve input. which is likely glutamatergic. The data suggest that the com- Octopus cells have an “on” response-a peak in activity fol- position of GIuRl-GIuR4 subunits on neurons in the cochlear lowed by variable levels of activity (Caspary, 1972)-and these nucleus may be related to presynaptic input; moreover, het- cells project to the ventral nucleusof the lateral lemniscus(Ad- erogeneous patterns of expression of the GIuR3 subunit, in ams, 1986) and the periolivary nuclei (Warr, 1966,1969,1983; addition, suggest that variability in mRNA levels within one Adams and Warr, 1976).The “chopper” responserecorded from population of morphologically defined cells is present. stellate neurons is also phasic, consisting of bursts of activity followed by inactivity; these cells project to the inferior collic- ulus (Adams, 1979). In the dorsal CN (DCN), the fusiform cell Received Aug. 25, 1992; revised Nov. 5, 1992; accepted Nov. 10, 1992. type also projects to the inferior colliculus (Adams, 1979); ex- We thank Dr. M. Bruce Warr for providing generous access to his archival histological slides of the rat cochlear nucleus, and Drs. J. C. Adams, V. Gallo, E. tracellular recordings of these cells show primarily a “pause? Mugnaini, A. Niedielski, and M. Schneider for their critical reviews of the manu- or “pauser buildup” responseconsisting of increasing levels of script. activity following a stimulus(Godfrey et al., 1975; Young, 1984). Parts of this article were presented in preliminary form at a NATO Advanced Research Workshop on the Mammalian Cochlear Nuclei: Organization and Func- While the auditory nerve suppliesthe major input to thesecells, tion, September 13- 17, 199 1. they also receive multiple inputs that are primarily inhibitory Correspondence should be addressed to Dr. Chyren Hunter, Section on Neu- rotransmitter Receptor Biology, Laboratory ofNeurochemistry, NIDCD, National from other neurons within the CN as well as from neurons in Institutes of Health, Building 36, Room SDOS, Bethesda, MD 20892. other brainstem nuclei (Cant and Mores& 1984). Copyright 0 1993 Society for Neuroscience 0270-6474/93/l 3 1932-15$05.00/O Extensive biochemical, pharmacological, physiological, and The Journal of Neuroscience, May 1993, 13(5) 1933 anatomical evidence suggests that glutamate, or a structurally over, we begin to define the nature of these postsynaptic recep- related compound, is the neurotransmitter of the auditory nerve tors. This analysis may also identify additional EAA pathways (Wenthold and Martin, 1984; Caspary et al., 1985; Altschuler in the CN. Since the auditory nerve innervates several mor- et al., 1986; Wickesburg and Oertel, 1989). Pharmacological phologically and physiologically distinct cell types, this analysis studies in chinchilla (Caspary, 1990) and chick (Nemeth et al., also addressesthe question of whether or not all neurons that 1983; Jackson et al., 1985) support the presence of a non-NMDA receive auditory nerve input expressthe same composition of receptor at the auditory nerve-CN synapse; rapid quisqualate-, GluRl-GluR4 subunits. AMPA-, or kainate (K&-evoked desensitizing currents, blocked by the non-NMDA antagonist 6-cyano-7-nitroquinoxaline-2,3 Materials and Methods dione (CNQX), characteristic ofAMPA/KA receptors, have also Oligonucleotide probes. Antisense oligonucleotide probes, 45 nucleo- been measured at the chick auditory nerve-CN synapse (Raman tides in length, were synthesized on an Applied Biosystems DNA syn- and Trussel, 199 1). Ligand-binding sites, in addition, show the thesizer and are identical to published oligonucleotide sequences se- presence of non-NMDA receptors in the CN (Baker and Glen- lected from the first cytoplasmic loop of the cDNAs encoding four denning, 199 1). NMDA receptors are also found in the CN, and AMPA-selective glutamate receptors, designated GluR 1, GluR2, GluR3, and GluR4 (also reported at GluR-A, GluR-B, GluR-C, and GluR-D, may be present on the same neurons that receive auditory nerve respectively; Keinlnen et al., 1990). Controls for hybridization selec- input (Monaghan et al., 1985). In addition to the auditory nerve tivity and specificity consisted of sense oligonucleotides to GluRl-GluR4 pathway, one additional glutamatergic pathway has been iden- cDNA, prepared from the identical regions used for antisense probes tified in the CN. The parallel fiber pathway originates with CN and hybridization with probes unrelated to GluR. All four GluR probes were labeled and processed simultaneously in each experiment to control granule cells and terminates on cartwheel, stellate, and fusiform for interexperimental variability. Oligonucleotides were purified and neurons of the DCN (Godfrey et al., 1977, 1978; Mugnaini et concentrated by gel electrophoresis and extracted with organic solvents. al., 1980b; Schwartz, 198 1; Oliver et al., 1983; Potashner, 1983; Purified oligonucleotides were 3’ end-labeled with terminal deoxynu- Oertel and Wu, 1989; Juiz et al., 1990; Manis, 1990). The other cleotidyl-transferase and 5’-YS-deoxyadenosine triphosphate (dATP) remaining synaptic populations in the CN have not been care- (New England Nuclear) for 5 min at 37°C and unincorporated label was extracted using organic solvents. fully characterized pharmacologically. In situ hybridization. Brainstems from male SpragueDawley rats, Multiple cDNAs for both non-NMDA and NMDA classes of 175-250 gm, were used. Tissue was rapidly removed, rinsed in phos- glutamate receptors have recently been identified. Based on se- phate-buffered saline (145 mM NaCl, 10 mM phosphate buffer, pH 7.5) quence homologies and pharmacological properties, the non- frozen, and stored at -80°C. Samples were sectioned at 16 pm and mounted on slides
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