Doctoral Dissertations

Weimin Zheng

Date of Award

8-1996

Degree Type

Dissertation

Degree Name

Doctor of Philosophy

Major

Life Sciences

Major Professor

Jim C. Hall

Committee Members

Christine R. Boake, Rebecca Prosser, James Lawler, G. Vaughan

Abstract

Neurons in the superior olivary nucleus (SON), an anuran (frog and toad) homologue of the superior olivary complex in mammals, exhibit a great degree of selectivity for the spectral components contained in the frog's acoustic communication sounds. Many of these frequency selective features are absent in the adjacent lower auditory nucleus, the dorsal lateral nucleus (DLN), and are likely created in the SON via interactions of excitatory and inhibitory inputs. Immunocytochemical studies have demonstrated the presence of the GABAergic and glycinergic cell bodies and terminals in the SON. GABA and glycine have been shown to be the predominant inhibitory neurotransmitters in the vertebrate brain. Thus, the SON provides a unique model for studying the neural mechanisms giving rise to frequency selectivity of the auditory neurons.

The main aim of the present study was to determine the roles of GABAergic and glycinergic inhibition in shaping the excitatory frequency tuning curves (eFTCs) and regulating the monaural response properties of neurons in the SON of the northern leopard frogs, Rana pipiens pipiens. The strategy used to achieve this goal was to block GABAergic and glycinergic inhibition in the SON pharmacologically by in vivo microiontophoresis of bicuculline (BIC) or strychnine (STR), selective antagonists for GABAA and glycine receptors, respectively. The effects of BIC and/or STR on the eFTCs, excitatory threshold, spontaneous firing rate, response magnitude, intensity-rate (IR) function, and temporal discharge pattern of SON cells were examined. The main findings are summarized as follows:

The general response properties of 329 SON neurons were studied using 118 leopard frogs. Summarizing: (1) Characteristic frequencies (CFs) of SON neurons ranged from 70 to 3000 Hz and were distributed over three frequency ranges: low- (70-599 Hz), middle- (600-1199 Hz), and high- (1200-3000 Hz) frequencies. (2) Five main types of eFTCs were observed for SON neurons: symmetrical, asymmetrical (including type I, II, and III), level-tolerant, closed, and bimodal (including type I and II). Of these, the symmetrical and the asymmetrical type I eFTCs resembled those seen at the levels of the DLN and the auditory nerve, whereas the remaining eFTC types were only observed in the SON. The discontinued bimodal eFTC, bimodal type II, has not been previously reported for SON neurons. (3) Two types of IR functions were obtained for the SON neurons: monotonic and nonmonotonic. (4) Five types of temporal discharge patterns were seen in the SON: primary-like, phasic-burst, phasic-burst plus sustained, phasic, and pauser. These discharge patterns displayed by SON cells resembled those seen in the frog DLN and in the mammalian superior olivary complex. In a small number of SON neurons, the temporal discharge patterns were stimulus intensity dependent. These results are in general agreement with those previously reported for SON neurons.

Iontophoretic application of BIC (1) broadened eFTCs in 51% of the cells tested; (2) changed eFTC configuration concomitant with broadening in 25% of the neurons studied; (3) elevated spontaneous firing rate in 34% of the cells examined; (4) decreased excitatory threshold at CF in 13% of the cells tested; (5) increased response magnitude to tone stimulus in 48% of the units examined; (6) rarely changed the shape of the intensity- rate function and the temporal discharge patterns; and finally (7) features of overall effects of BIC application in individual neurons distinguished eight group of SON cells showing unique combination of response properties changes induced by BIC application. ,p>Iontophoretic application of STR (1) broadened eFTCs in 7% of the cells tested; (2) decreased threshold at CF in 4% of the cells studied; (3) elevated spontaneous firing rate in 10% of neurons tested; and (4) increased response magnitude in 12% of the cells examined. These results were consistent with known antagonistic effects of STR on the glycine receptors in the brain.

In contrast, iontophoretic application of STR also (1) narrowed eFTCs in 19% of the cells studied; (2) increased threshold at CF in 13% of cells tested; (3) suppressed spontaneous firing rate in 40% of neurons studied; (4) decreased response magnitude in 33% of neurons examined; (5) changed the shape of intensity-rate function by inhibiting discharge rate in 7% of the cells tested; and (6) altered the temporal discharge pattern by suppressing cell's response in 2% of units examined. Several possible mechanisms underlying the inhibitory effects of STR on the activity of SON neurons were examined and discussed. The most likely mechanism supported by experimental results is synaptic interaction between glycinergic and GABAergic neurotransmission, i.e., pre-synaptic inhibition of GABAergic neurons by glycinergic neurons.

Based on these results, it was concluded that (I) GABA and glycine function as inhibitory neurotransmitters in the SON of frogs; (II) GABAergic inhibitions play an important role in (a) the creation of frequency selective features of the SON neurons, (b) modulation of neuronal sensitivity, (c) neural gain control, and (d) signal amplitude coding; (III) Glycinergic inhibition also plays similar roles to those of GABAergic inhibitions, but it does so either directly in a small population of SON cells or, more frequently, indirectly via pre-synaptic inhibition GABAergic neurons; and (IV) Multiple GABAergic and/or glycinergic circuits operate to shape eFTCs and response properties of SON neurons. Several specific neural circuits involving GABAergic inhibition were proposed to account for each of the eight combinations of response property changes induced by iontophoretically applied BIC.

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