THE ROLES OF GABAERGIC AND GLYCINERGIC INHIBITION ON BINAURAL PROCESSING IN THE DORSAL NUCLEUS OF THE LATERAL LEMNISCUS OF THE MOUSTACHE BAT

1. We studied the monaural and binaural response properties of 99 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat before and during the iontophoretic application of antagonists that blocked gamma-aminobutyric acid-A (GABA(A)) receptors (bicuculline) or glycine receptors (strychnine). All cells were driven by monaural stimulation of the contralateral ear, whereas monaural stimulation of the ipsilateral ear never evoked discharges. The binaural properties of 81 neurons were determined by holding the intensity constant at the contralateral ear and presenting a variety of intensities to the ipsilateral ear. This procedure generated interaural intensity disparity (IID) functions and allowed us to determine the effect of ipsilaterally evoked inhibition on a constant excitatory drive evoked by the contralateral ear. 2. One of the main findings is that the IID functions in the majority of DNLL neurons were not affected by application of either strychnine or bicuculline. Blocking glycinergic inhibition with strychnine had no effect on the IID functions in 75% of the cells studied. However, strychnine did change the IID functions in similar to 25% of the DNLL population. In those cells glycinergic inhibition appeared to be partially, or, in a few cases, entirely responsible for the ipsilaterally evoked spike suppression. In contrast, blocking GABAergic inhibition with bicuculline had no discernible effect on the ipsilaterally evoked spike suppression in any of the excitatory/inhibitory cells that we recorded. GABAergic inhibition, therefore, plays no role in the formation of IID functions of neurons in the DNLL. Furthermore, the results suggest that glycinergic inhibition also does not contribute to the suppression of spikes evoked by stimulation of the contralateral ear in the vast majority of DNLL neurons. 3. Although the majority of IID functions were not influenced when either GABAergic or glycinergic innervation was blocked, ipsilateral stimulation alone evoked both a glycinergic and GABAergic inhibition in most DNLL cells. These inhibitory events were demonstrated in 18 other cells by evoking discharges with the iontophoretic application of glutamate. Stimulating the ipsilateral ear alone under these conditions caused a suppression of the glutamate-evoked discharges. Furthermore, the spike suppression persisted for a period of time that was longer than the duration of the tone burst at the ipsilateral ear. 4. The application of bicuculline or strychnine had different effects on the glutamate-elicited spikes. Bicuculline reduced the duration of the inhibition, and it was always the latter portion of the inhibition that was abolished by bicuculline. In more than half of the cells studied strychnine also reduced the duration of the inhibition. However, strychnine always abolished an early component of the inhibition. In many cells the ipsilaterally evoked inhibition of the glutamate-elicited spikes was completely abolished when bicuculline and strychnine were applied simultaneously. 5. The results from blocking GABAergic or glycinergic innervation on the IID functions and those from the studies of glutamate-elicited discharges can be reconciled when one considers the push-pull effects of binaural simulation on the ipsilateral and contralateral lateral superior olives (LSOs) and their influences on the DNLL. The hypothesis is that IIDs that favor the contralateral ear drive the contralateral LSO. That LSO then drives cells in the DNLL via a crossed excitatory projection. In contrast, IIDs that favor the ipsilateral ear inhibit the contralateral LSO but also drive the ipsilateral LSO. The driven activity from the ipsilateral LSO has two principal effects. The first is that it provides a glycinergic inhibition to the DNLL from which we were recording, thereby evoking a short-latency inhibition. The second effect is to provide an excitatory input to the DNLL on the opposite side, thereby exciting those DNLL cells. Those DNLL cells then provide a GABAergic input to the DNLL via the commissure of Probst. The latency of the GABAergic inhibition is longer than that of the glycinergic inhibition because of the additional synapse in the circuit. The significant feature of the above hypothesis is that the two inhibitory effects are only evoked by IIDs that completely suppress the contralateral LSO. Thus the inhibition from the glycinergic and GABAergic projections is imposed on a DNLL cell that is receiving no excitation, but rather whose membrane potential is at a resting value. Because there was no excitation, and thus no driven rate that could be reduced by the inhibition, these inhibitory events were not apparent when viewed through an extracellular electrode that only recorded action potentials.