Different coding strategy of sound information between GABAergic and glutamatergic neurons in the auditory midbrain

Key points: In the central nucleus of the inferior colliculus (ICC), which acts as the hub of the auditory pathways, how the sound is coded by distinct cell types is largely unknown. Large GABAergic cells are tuned broadly to pure tones and respond more strongly to frequency-modulated sweeps than small GABAergic and glutamatergic (GLU) cells. Neurons, especially GLU cells, which share sharpness of tuning and sweep sensitivity, were spatially clustered inside the ICC. The difference in responsiveness between cell types was partially explained by the morphology of dendritic trees and the spatial distributions of excitatory and inhibitory inputs. The results suggest that each ICC cell type has a particular sound-encoding strategy, which is partially determined by the morphological characteristics and location of cells, and contributes information coding in higher centres in different ways. Abstract: The rules governing the encoding of sound information in the higher auditory centres are largely unknown. In the central nucleus of the inferior colliculus (ICC), which acts as the hub of the auditory pathways, the presence of functional maps other than tonotopicity has been suggested but not established, due to significant heterogeneity in the response properties of single microdomains. Since each ICC cell type has distinct neuronal circuitry, each cell type might encode sound information differently. Here, juxtacellular recording from rat ICC of both sexes revealed that large GABAergic (LG), small GABAergic (SG) and glutamatergic (GLU) cells encode sound information differently. LG cells are broadly tuned and respond more strongly to frequency-modulated sweeps than SG and GLU cells. At a population level, responsiveness to sweeps is location dependent: the responsiveness to sweeps is shared in local clusters of GLU cells, whereas that to directional selectivity of sweeps is shared in local clusters of LG cells. The difference in responsiveness between cell types was partially explained by the morphology of dendritic trees and the spatial distributions of excitatory and inhibitory inputs. LG neurons had a dense local axonal plexus with projection fibres to multiple distant targets, whereas GLU projection neurons mainly aimed at a single, distant target and had less dense local collaterals. These results suggest that each ICC cell type has a particular sound-encoding strategy, which is partially determined by the morphological characteristics and location of the cell, and the different cell types contribute information coding in higher centres in different ways.