GABAERGIC CIRCUITS SHARPEN TUNING CURVES AND MODIFY RESPONSE PROPERTIES IN THE MOUSTACHE BAT INFERIOR COLLICULUS

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-aminobutyric 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. The bicuculline induced changes in rate-level function and temporal response pattern, or absence of any change, occurred both in cells whose tuning curves widened with bicuculline and in cells whose tuning curves did not expand. 5. The results suggest a variety of GABAergic circuits operate to shape the frequency tuning and the response properties of collicular neurons. The neurons in some GABAergic circuits have best frequencies that flank the best frequency of the excitatory projections. The inhibition evoked by these circuits is sufficiently strong to completely suppress discharges evoked by those frequencies of the excitatory tuning curve with which the inhibitory tuning curves overlap. These circuits thereby sharpen the tuning curves of their targets in the colliculus. The GABAergic neurons in other circuits have best frequencies that are in register with the best frequencies of the excitatory projections. The inhibitory projections in these circuits reduce the discharge rate and shape the discharge properties evoked by the excitatory projections. Presumably both types of circuits, or an intermediate type can contact the same neuron, resulting in a tuning curve that is sharpened and response properties within the tuning curve that are modified.