Iontophoresis In Vivo Demonstrates a Key Role for GABAA and Glycinergic Inhibition in Shaping Frequency Response Areas in the Inferior Colliculus of Guinea Pig

The processing of biologically important sounds depends on the analysis of their frequency content by the cochlea and the CNS. GABAergic inhibition in the inferior colliculus shapes frequency response areas in echolocating bats, but a similar role in nonspecialized mammals has been questioned. We used the powerful combination of iontophoresis with detailed analysis of frequency response areas to test the hypothesis that GABAergic and glycinergic inhibition operating in the inferior colliculus of a nonspecialized mammal (guinea pig) shape the frequency responses of neurons in this nucleus. Our analysis reveals two groups of response areas in the inferior colliculus: V-shaped and non-V-shaped. The response as a function of level in neurons with V-shaped response areas can be either monotonic or nonmonotonic. Application of bicuculline or strychnine in these neurons, to block inhibition mediated by GABAA or glycinergic receptors, respectively, increases firing rate primarily within the boundaries of the control response area. In contrast, neurons in the non-V-shaped group have response areas that include narrow, closed, tilted, and double-peaked types. In this group, blockade of GABAA and glycine receptors increases firing rate but also changes response area shape, with most becoming more V-shaped. We conclude that (1) non-V-shaped response areas can be generated by GABA and glycinergic synapses within the inferior colliculus and do not simply reflect inhibition acting more peripherally in the pathway and (2) frequency-dependent inhibition is an important general feature of the mammalian inferior colliculus and not a specialization unique to echolocating bats.

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