Contribution of GABAergic inhibition to the response characteristics of auditory units in the avian forebrain.

1. We tested the contribution of GABAergic inhibition to the response characteristics of 213 neurons in the auditory telencephalon of chronically prepared nonanesthetized chickens. Extracellular recordings were obtained with multibarrel glass electrodes containing a tungsten wire. Auditory stimuli consisted of tones, two-tone combinations, and noise bursts presented either free field or via earphones. 2. Response properties of the neurons were studied both before and during iontophoretic application of GABA, glutamate, bicuculline methiodide (BIC), and acetylcholine. 3. During BIC application excitatory responses were facilitated. With the exception of transient off-responses, which occasionally appeared only in the BIC condition, the temporal response patterns to tone stimuli at the units' best frequency usually were unaltered. In no case was an inhibitory response component to binaurally presented pure tones antagonized by BIC. 4. BIC iontophoresis enlarged the isointensity-response areas of the vast majority of neurons in the structures of the auditory forebrain lying postsynaptic to the thalamorecipient layer L2. This effect was not obtained when neurons were depolarized to perithreshold levels with glutamate. 5. Two-tone stimulation resulted in a suppression of the excitatory response to a neuron's best frequency when the second frequency lay outside the excitatory response area. In lamina L2, the frequency range inducing two-tone suppression was narrow, and the suppressive effect was not antagonized by BIC. In the postsynaptic layers, frequencies up to three octaves from the neurons' best frequency induced two-tone suppression that was sensitive to BIC. In addition, these neurons also displayed a BIC-insensitive suppression similar to the one seen in layer L2. 6. Neurons displaying no or only a poor response to white-noise stimulation strongly responded to this wide-band stimulus during BIC iontophoresis. 7. Neurons without tone responses usually displayed clear response areas to tones during BIC application. Iontophoretic application of acetylcholine, but not glutamate, also induced such tone responses. Two-tone combinations with frequencies lying within the response areas observed in the BIC condition elicited excitatory responses after full recovery from the BIC application. 8. During BIC iontophoresis nonmonotonic intensity-response functions were converted to monotonic functions in most of the neurons studied. 9. A model of GABAergic inhibitory interactions is proposed that is based on two independent GABAergic systems.(ABSTRACT TRUNCATED AT 400 WORDS)