Located in the ventrolateral region of the avian brainstem, the superior olivary nucleus (SON) receives inputs from nucleus angularis (NA) and nucleus laminaris (NL) and projects back to NA, NL, and nucleus magnocellularis (NM). The reciprocal connections between the SON and NL are of particular interest because they constitute a feedback circuit for coincidence detection. In the present study, the chick SON was investigated. In vivo tracing studies show that the SON projects predominantly to the ipsilateral NM, NL, and NA. In vitro whole-cell recording reveals single-cell morphology, firing properties, and postsynaptic responses. SON neurons are morphologically and physiologically suited for temporal integration; their firing patterns do not reflect the temporal structure of their excitatory inputs. Of most interest, direct stimulation of the SON evokes long-lasting inhibition in NL neurons. The inhibition blocks both intrinsic spike generation and orthodromically evoked activity in NL neurons and can be eliminated by bicuculline methiodide, a potent antagonist for GABAA receptor-mediated neurotransmission. These results strongly suggest that the SON provides GABAergic inhibitory feedback to laminaris neurons. We discuss a mechanism whereby SON-evoked GABAergic inhibition can influence the coding of interaural time differences for sound localization in the avian auditory brainstem.

1. The influence of bicuculline on the tuning curves of 65 neurons in the inferior colliculus of the mustache bat was investigated. Single units were recorded with multibarrel electrodes where one barrel contained bicuculline, an antagonist specific for gamma-amino-butyric acid (GABA)A receptors. Fifty-nine tuning curves were recorded from units that were sharply tuned to 60 kHz, the dominant frequency of the bat's orientation call, but six tuning curves were also recorded from units tuned to lower frequencies and whose tuning curves were broader than the 60 kHz cells. Tuning curves were constructed from peristimulus time (PST) histograms obtained over a wide range of frequency-intensity combinations. Thus tuning curves, PST histograms evoked by frequencies within the tuning curve, and rate-level functions at the best frequency were obtained before iontophoresis of bicuculline and compared with the tuning curves and response properties obtained during the administration of bicuculline. 2. Three general types of tuning curves were obtained: 1) open tuning curves that broadened on both the high- and low-frequency sides with increasing sound level; 2) level-tolerant tuning curves in which the width of the tuning curve remained uniformly narrow with increasing sound level; and 3) upper-threshold tuning curves, which did not discharge to high-intensity tone bursts at the best frequency, thereby creating closed or folded tuning curves. 3. One major finding is that GABAergic inhibition plays an important role in sharpening frequency tuning properties of many neurons in the mustache bat inferior colliculus. In response to blocking GABAergic inputs with bicuculline, the tuning curves broadened in 42% of the neurons that were sharply tuned to 60 kHz. The degree of change in most units varied with sound level: tuning curves were least affected, or not affected at all, within 10 dB of threshold and showed progressively greater changes at higher sound levels. These effects were seen in units that had open, level-tolerant, and upper-threshold tuning curves. 4. A second key result is that bicuculline affected rate-level functions and/or temporal discharge patterns in many units. Bicuculline transformed the rate-level functions of 13 cells that originally had nonmonotonic rate level functions, from strongly nonmonotonic into weakly nonmonotonic or monotonic functions. It also changed the temporal discharge patterns in 22 cells, and the changes were often frequency specific.(ABSTRACT TRUNCATED AT 400 WORDS)

In the avian auditory brainstem, nucleus magnocellularis (NM) functions to relay phase-locked signals to nucleus laminaris for binaural coincidence detection. Although many studies have revealed that NM neurons exhibit intrinsic physiological and anatomical specializations for this purpose, the role of inhibition has not been fully explored. The present study characterizes the organization of GABAergic feedback to NM. Anterograde and retrograde labeling methods showed that NM receives a prominent projection from the ipsilateral superior olivary nucleus (SON). The functional features of this projection were explored in a brain slice preparation. Stimulating fibers from the SON evoked long-lasting, depolarizing responses in NM neurons that were blockable by bicuculline, a GABA(A) receptor antagonist. The slow time course of these responses allowed them to undergo temporal summation during repetitive stimulation. The summed GABAergic response was capable of blocking spikes generated in NM neurons by suprathreshold current injection. This inhibitory effect was attributable to a large reduction in input resistance caused by a combination of the opening of a GABAergic Cl(-) conductance and the recruitment of a low-voltage activated K(+) conductance. This large reduction of input resistance increased the amount of current necessary to drive NM neurons to threshold. The results lead us to propose that GABAergic inhibition enhances phase-locking fidelity of NM neurons, which is essential to binaural coincidence detection in nucleus laminaris.

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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 (GABAA) 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 approximately 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.(ABSTRACT TRUNCATED AT 400 WORDS)