THE JOURNAL OF COMPARATIVE NEUROLOGY :J4S:40;3-41S (1994) GABAergic Terminals in Nucleus Magnocellularis and Laminaris Originate From the Superior Olivary Nucleus E.A. LACHlCA, R. RUBSAMEN, AND E.W RUBEL Virginia Merril Bloedel Hearing Research Center, Department ofOtolaryngology- Head and Neck Surgery, University ofWashington, Seattle, Washington 98195 ABSTRACT The auditory brainstem nuclei, angularis (NA),magnocellularis (NMl,and laminaris (NLl of the chicken, Gallus, contain terminals that stain for antibodies against the inhibitory neurotransmitter, gamma-aminobutyric acid (GABA).Some ofthese terminals originate from cells surrounding nucleus magnocellularis. Results from this study indicate that the majority of the GABAergic terminals found in NA,NM and NL originate from the superior olivary nucleus (SON). Injections of cholera toxin and horseradish peroxidase show that superior olivary nucleus (SON) neurons, which respond to pure tones, project bilaterally to NA,NM and NL.NA and NL are reciprocally connected with the SON. More NA cells project to the SON than NL cells. While SON neurons project to NM, NM neurons do not project axons back to the SON. The configuration of SON terminals in NA, NM and NL matches the pattern of GABA- immunoreactive puncta seen in these three nuclei: they surround individual NM cells, congregate in the dendritic neuropil ofNL, and blanket the NA.The data indicate that NA,NM and NL may be affected by two different inhibitory cell types: local interneurone and SON neurons. Patterns of connectivity described in this report suggest that the activity ofNA cells could influence NM and NL cell physiology. Specifically, increases in NA cell activity could augment the effects ofGABAergic SON neurons on NM and NL. Hence, binaural perception in the chicken may be more dependent upon changes in intensity cues than previously believed. 1994 Wiley-Liss, Inc. Keywords: parallel pathways, cochlear nucleus, inhibition, auditory system, cholera toxin fo;n avi~ns, ax?n~ from the auditory nerve bifurcate to 1 m excItatory ipsilateral connections with the large round ce I. hs III nucleus magnocellularis (NM) and the stellate- ~apedcellslocated in nucleus angularis (NA;Boord, 1969; arksand Rubel, 1978; Jhaveri and Morest, 1982a,b). NM ~urons project bilaterally to nucleus laminaris (NL), a s :;etofcells whose dendritic branches are polarized dor- ;a ! and ventrally (Boord, 1969; Parks and Rubel, 1975; a~lth a.nd~ubel, 1979; Young and Rubel, 1983). Ipsilat~r- thY projectmg N.Maxons form excitatory connections WIth e.dorsaldendntes oflaminaris cells while contralaterally project' 11 ' . .h mg co ateral branches form oxcitatory synapses 7~~ . the ventrally directed dendrites (Rubel and Parks, p .5,Young and Rubel, 1983, 1986). NA neurons do not t .rOjectto NL. Instead, their ascending axons form connec- lonsw'th T k I .anumber ofstructures (Conlee and Parks, 1986; W~i~~Shl and Konishi, 1988b), the most prominent of 1t ISthe dorsal lateral mesencephalic nucleus (MLd). t nercalated among the excitatory connections made be- e;~en the auditory nerve and NM and NA neurons, and CItatoryconnections between NM axons and NL neurons, 1994WILEY-LISS, INC. is a dense network ofterminals containing the inhihitory neurotransmitter, gamma-aminobutyric acid,GABA(Code et al., 1989; Carr et al., 1989; von Bartheld et al., 19891. Where dothese GABA-containing terminals originate from? Results from a previous study from our laboratory re- vealed that stellate cells surrounding the chicken NM and NL stained positively for GABA (von Bartheld et al., 1989). A similar distribution of GABA-immunoreactive interneu- rons has also been described in the barn owl (Carr et al., 1989). It has been argued that these cells provide some of the GABAergic terminations ending on magnocellularis and laminaris neurons. This small population of GABA- staining neurons may not account completely for the dense network of terminals present in NM and NL. GABA- positive terminals are also present in NA,and the origin of these terminals isnot known. Accepted April 18, 1994. Address reprint requests to E.W Rubel, Virginia Merril Hearing Research Center, Department of Otolaryngology-Head and Neck Surgery, University ofWashington, Seattle, WA 98195.