GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus

Abstract

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)

Intracellular Recordings in Response to Monaural and Binaural Stimulation of Neurons in the Inferior Colliculus of the Cat

“…A similar observation has been made in the IC of the bat (Covey et al, 1996). Pharmacological studies have shown that GABA or glycine blockers can broaden the frequency tuning of IC neurons, indicating that side band suppression is via inhibitory mechanisms (Vater et al, 1992;Yang et al, 1992). Interaural delay curves generated from the response to the binaural-beat stimulus (for details, see Yin and Kuwada, 1983;Kuwada et al, 1987).…”

Spectrotemporal Receptive Fields in the Inferior Colliculus Revealing Selectivity for Spectral Motion in Conspecific Vocalizations

“…One explanation for this difference in the effects of inhibition on direction selectivity and inseparability is that blocking inhibition frequently causes an expansion of the excitatory receptive field, in which the expansion is not uniform along the spectrotemporal axis (Yang et al, 1992;Palombi and Caspary, 1996;LeBeau et al, 2001;Klug et al, 2002). Such a nonuniform expan- 6.…”

Functional magnetic resonance imaging measurements of sound-level encoding in the absence of background scanner noise

“…Thus, the physiological response to increasing sound level also involves inhibition of the activity of narrow-band, low intensity-sensitive neurones. Such inhibition is in evidence from the dorsal cochlear nucleus all the way up to the cortex and there are certainly local inhibitory contributions to non-monotonicity at least as high as the inferior colliculus (Yang et al, 1992). At the cortical level, there are profuse local inhibitory influences (Cox et al,.…”