Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus.

Abstract

1. We examined the role of gamma-aminobutyric acid (GABA)-mediated inhibition in shaping excitatory tuning curves and creating selectivity for frequency-modulated (FM) sweeps in 29 neurons in the central nucleus of the inferior colliculus (ICC) of the pallid bat, with the use of single-unit recording coupled with the iontophoretic application of bicuculline methiodide (BIC), an antagonist of GABAA receptors. 2. BIC increased response magnitude 2 to 6 times over pretreatment levels in > 80% of neurons tested, and converted > 50% of nonmonotonic intensity-rate functions to monotonic or plateaued functions, demonstrating that GABAergic input normally limited response magnitude and inhibited responses at higher intensities. BIC typically had little effect on response thresholds, except in more specialized neurons that normally responded poorly to tones. In these cases, BIC disinhibited the neurons' responses to tones and lowered excitatory thresholds as much as 25 dB. 3. We examined the effects of BIC application on both excitatory and inhibitory tuning curves (measured with simultaneous 2-tone inhibition) to determine whether inhibitory curves were GABA mediated and whether removal of this inhibition was accompanied by an expansion of the excitatory curve. BIC had variable effects on the width of excitatory curves. In most cases, excitatory curves were at least slightly broadened, and expanded into regions previously occupied by inhibitory curves. In most cases, excitatory curves were at least slightly broadened, and expanded into regions previously occupied by inhibitory curves. However, in a few cases, inhibitory curves could be eliminated without an expansion of the excitatory curve. The greatest effect was seen in neurons with closed excitatory tuning curves; blocking GABAergic input caused the curves to open, allowing the neurons to respond at higher intensities. 4. Approximately 50% of the neurons in the ICC tuned to the spectrum of the bat's downward FM sweeping biosonar pulse respond preferentially to downward FM sweeps and not to upward sweeps, tones, or noise. In all neurons tested, BIC at least partially destroyed selectivity for sweep direction. This destruction could occur, however, without a loss of response exclusivity; in some cases, the neurons still did not respond to tones or noise. These results suggest that response selectivity for a species-specific signal is created by GABAergic input to ICC neurons. These results are used to suggest a mechanism that creates selectivity for FM sweep direction.