1. Recent studies have suggested that gamma-aminobutyric acid (GABA) inputs shape monaural and binaural neuronal response properties in the central nucleus of the inferior colliculus (CIC). CIC neurons receive major inhibitory GABAergic projections from intrinsic, commissural, and extrinsic sources. Many GABAergic projections now are thought to arise from cells that are tonotopically matched to their CIC targets. 2. We tested the hypothesis that GABA circuits are aligned primarily within the CIC target neuron's excitatory response area and therefore have their greatest effects on discharge rate mainly within that frequency domain. GABA inhibition was examined by recording families of isointensity contours before, during, and after GABAA receptor blockade. Iontophoretic application of bicuculline-methiodide (BMI) was used to block GABAA receptors. Quantitative measures of frequency bandwidth and z-score analysis of discharge rate within the excitatory receptive field were used to compare pre- and postdrug conditions. 3. Chinchilla CIC unit response properties were similar to those described for other species, with a high percentage of phasic temporal response patterns and nonmonotonic rate-intensity functions in response to monaural contralateral characteristic frequency (CF) tones. Binaural responses of most CIC neurons showed suppression of contralaterally evoked responses by ipsilateral stimulation. 4. For 85% of CIC neurons, blockade of GABAA inputs was found to increase discharge rate within the excitatory response area. Forty-five percent were classified as near-CF changes and 32% as near-CF and low side. Changes in lateral/flanking inhibition in the absence of near-CF changes were never observed. Forty-one percent of CIC neurons displayed less than a 10% increase in frequency bandwidth at 25-35 dB above threshold with BMI application. 5. These data suggest that GABA inhibition arises primarily from neurons with inhibitory fields aligned with their CIC targets. Thus the effect of the inhibition is primarily contained within or overlapping each target neuron's excitatory response area. CIC GABAergic circuits may function to adjust the gain needed for coding complex signals over a wide dynamic range.
1. The amino acid neurotransmitters gamma-aminobutyric acid (GABA) and glycine function as inhibitory neurotransmitters associated with nonprimary inputs onto spherical bushy and stellate cells, two principal cell types located in the anteroventral cochlear nucleus (AVCN). These neurons are characterized by primary-like (including phase-locked) and chopper temporal response patterns, respectively. 2. Inhibition directly adjacent to the excitatory response area has been hypothesized to sharpen or limit the breadth of the tonal frequency receptive field. This study was undertaken to test whether GABA and glycine circuits function primarily to sharpen the lateral edges of the tonal excitatory response area or to modulate discharge rate within central portions of the excitatory response area of AVCN neurons. 3. To test this, iontophoretic application of the glycineI antagonist, strychnine, or the GABAA antagonist, bicuculline, was used to block inhibitory inputs after obtaining control families of isointensity contours (response areas) from extracellularly recorded AVCN neurons. 4. Blockade of GABA and/or glycine inputs was found to increase discharge rate primarily within the excitatory response area of neurons displaying chopper and primary-like temporal responses with little or no change in bandwidth or in off-characteristic frequency (CF) discharge rate. 5. The principal sources of inhibitory inputs onto AVCN neurons are cells located in the dorsal cochlear nucleus and superior olivary complex, which appear to be tonotopically matched to their targets. In agreement with these morphological studies, the data presented in this paper suggest that most GABA and/or glycine inhibition is tonotopically aligned with excitatory inputs. 6. These findings support models that suggest that GABA and/or glycine inputs onto AVCN neurons are involved in circuits that adjust gain to enable the detection of signals in noise by enhancing signal relative to background.
1. Presbycusis, age-related hearing loss, is an ever increasing problem in our aging society. It involves changes in both the peripheral and central portions of the auditory system. The inferior colliculus (IC) has been shown to display age-related changes including decreased gamma-aminobutryic acid (GABA) levels, decreased glutamate decarboxylase levels, and decreased binding by GABAB receptors, as well as rearrangement of axon terminals in aging Fischer 344 (F344) rats. Age-related physiological changes have also been noted in the ICs of C57 and CBA mice. 2. Given the age-related alterations in the inhibitory neurotransmitter system, we hypothesized that aged F344 rats would show alterations in the physiological response properties of their IC neurons due to an imbalance in the relative levels of inhibition and excitation affecting the neuronal firing. 3. In vivo extracellular single-unit recordings were made from 297 IC neurons in ketamine/xylazine-anesthetized aged (24 mo) F344 rats. Locations of recorded units were determined from the electrode track marks and horseradish peroxidase marks. Results were compared with those obtained from young adult (3 mo) animals. 4. Average threshold increased from 25.4 dB SPL in young rats to 56.1 dB SPL in aged rats. 5. Although there was a reduction in the percentage of units recorded at either extreme of the frequency range in aged animals, the characteristic frequency (CF) range and mean did not differ between the two groups. 6. For the IC as a whole, no differences were noted in spontaneous activity, first spike latency, dynamic range, percentage of units with nonmonotonic contralateral CF tone rate/intensity functions (RIFs), or percentage of units sensitive to change in CF tone presentation rate. 7. In aged rats, a higher percentage of units was poorly responsive to auditory stimulation. 8. In the aged rat, there was a 12% reduction in the maximum discharge rate, a 12% increase in the percentage of units classified as onset in their temporal response pattern, and an 18% increase in the breadth of the isointensity functions at 30 dB above threshold. 9. Age-related changes in the central nucleus of the IC (CIC) frequently differed from those observed in the external cortex of the IC (ECIC). The percentage of units classified as having nonmonotonic contralateral tone RIFs decreased with age in the CIC but increased with age in the ECIC, and the percentage of units classified as onset in their temporal response pattern increased with age in the CIC but did not change with age in the ECIC. 10. The results of this study support the hypothesis that there is an age-related shift to higher intensities in the working range of most CIC units along with a small, selective deficit in inhibitory processing. When considered in conjunction with the mouse aging studies conducted by other researchers and with the results of a similar study of single units in the visual system (lateral geniculate nucleus) of young and aged rhesus monkeys, these results suggest that compensatory mechani...
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