GABA is involved in spatial unmasking in the frog auditory midbrain

Abstract

Real-world listening situations comprise multiple auditory objects. Sounds originating from different objects are summated at the eardrum. The auditory system therefore must segregate the streams of sounds associated with the different objects. One listening strategy in complex environments is to attend to signals originating from one spatial location. In doing so, signal detection is compromised when a masker is present at close proximity, and detection is improved if the masker is spatially separated from the signal. A recent study has shown that, in frogs, spatial unmasking is more robust at the midbrain than at the periphery, indicating the importance of central mechanisms for this process. In this study, we investigated spatial unmasking patterns of single neurons in the frog inferior colliculus (IC) before and during iontophoretic application of bicuculline, a GABA(A) receptor antagonist. We found that drug application markedly decreased the strength of spatial unmasking such that even large angular separation of signal and masker sources produced only a weak masking release. Under the drug, the strength of spatial unmasking of midbrain neurons approximated that of auditory nerve fibers. These data show that GABAergic interactions in the auditory midbrain play an important role in spatial unmasking. Analysis of the effect of the drug on the direction sensitivity of the units shows that for the majority of IC units, bicuculline degrades binaural processing involved in directional coding, thereby compromising spatial unmasking. For other IC units, however, the decline in the strength of spatial unmasking is attributable to the effects of bicuculline on different central auditory processes.

Figure 1.

Mating trills of Rana pipiens (or the probe) and the masker used in this study. A, Power spectrum of the probe at 63 dB SPL. B, Power spectrum of masker at 69 dB SPL. C, Power spectrum of probe and masker at respective levels, i.e., at a signal-to-noise ratio of -6 dB. D, Waveform of the probe in its digitized form. E, Waveform of the masker in its digitized form.

Figure 2.

Rate level functions (left plots), d′ functions (middle plots), and composite dot histograms (right plots) of an IC unit to P alone (A) and P + M (B). In the left plots, the response of the unit at each sound level is shown by the average spike count ± SD to 10 stimulus (Stim.) epochs. In the middle plots, the y-axis represents d′ (for calculation, see Materials and Methods), and the open arrows indicate the probe detection thresholds to P alone (18.3 dB SPL) and P + M (21.2 dB SPL), namely, the sound levels at which d′ = 1; the corresponding levels are shown by solid arrows in the left plots and by open arrowheads in the right plots. The composite dot histograms in the right plots show the timing of trains of action potentials (each spike is represented by a single dot) at various sound levels. Time 0 represents the onset time of the acoustic stimuli. In these plots, 10 traces of spike trains are shown at each sound level.

Figure 3.

Spatial unmasking response patterns of unit 28-2 (best frequency, 700 Hz). A, RLF of the unit to P alone at c90° (this RLF is also shown in B-F as a dotted curve); the open arrow indicates the probe detection threshold to this stimulus as determined by d′ of 1. B-F, MRLFs to P + M (solid curve) at various masker azimuths; for each plot, the filled arrow indicates the probe detection threshold for P + M (i.e., the sound level for which d′= 1). G, Change in the probe detection threshold as a result of masking and spatial unmasking (through angular separation of P and M sources) during the control period before drug application; the diamond represents the probe detection threshold for P alone; X, amount of threshold elevation attributable to masking; Y, maximum masking release attributable to source separation. H-N, Response characteristics of the unit during the period when bicuculline was applied iontophoretically (15 nA). O, Spatial unmasking response pattern of the unit 40 min after withdrawal of bicuculline.

Figure 4.

Spatial unmasking response patterns of four representative IC neurons. See legend to Figure 3 for the different symbols. A, B, Data from two units with graded spatial unmasking patterns under the control (i.e., predrug) and experimental (i.e., when BIC was applied iontophoretically) conditions. C, D, Responses of two units with J-type spatial unmasking patterns under the control condition.

Figure 5.

Distributions of threshold shift attributable to masking and the maximum masking release attributable to spatial separation for 28 IC units studied under two different experimental conditions. The mean ± SD of each data set are shown above each graph. The results of two-tailed Student's t tests between the same data set from two different experimental conditions are shown in B and D. N.S., Not statistically significant. **Statistically significant difference.

Figure 6.

Amount of threshold shift (A) and maximum masking release (B) for each of the 28 IC units under the normal (left side) and experimental (right side) conditions. Open circles in B represent the data from five IC units that were minimally affected by drug application.

Figure 7.

Directional responses of two IC units to M alone at a suprathreshold level during the control (open circle) and experimental (filled circle) conditions. A, B, Directional responses from a unit whose directional sensitivity was reduced by application of BIC, using the absolute spike count and normalized response (with regard to the maximum spike count for the respective response curve) as a metric. C, D, Similar data from a unit whose directional sensitivity was increased by application of BIC.

Figure 8.

Effects of drug application on the directional sensitivity and spatial unmasking of IC units. Directional sensitivity was measured by the total percent change in normalized directional responses between c90 and i90° (see Fig. 7). The x-axis shows the difference in the maximum masking release (see Figs. 3, 4, Y) between the control and experimental conditions, with negative values indicating a decrease in masking release resulting from drug application. The y-axis shows the difference in the percent change in the directional sensitivity of the unit between the control and experimental conditions; negative and positive values indicate, respectively, a decrease and increase in directional sensitivity resulting from drug application.