Development of Intrinsic Connectivity in the Central Nucleus of the Mouse Inferior Colliculus

The inferior colliculus (IC) in the mammalian midbrain is the major subcortical auditory integration center receiving ascending inputs from almost all auditory brainstem nuclei as well as descending inputs from the thalamus and cortex. In addition to these extrinsic inputs, the IC also contains a dense network of local, intracollicular connections, which are thought to provide gain control and contribute to the selectivity for complex acoustic features. However, in contrast to the organization of extrinsic IC afferents, the development and functional organization of intrinsic connections in the IC has remained poorly understood. Here we used laser-scanning photostimulation with caged glutamate to characterize the spatial distribution and strength of local synaptic connections in the central nucleus of the inferior colliculus of newborn mice until after hearing onset (P2-P22). We demonstrate the presence of an extensive excitatory and inhibitory intracollicular network already at P2. Excitatory and inhibitory synaptic maps to individual IC neurons formed continuous maps that largely overlapped with each other and that were aligned with the presumed isofrequency axis of the central nucleus of the IC. Although this characteristic organization was present throughout the first three postnatal weeks, the size of input maps was developmentally regulated as input maps underwent an expansion during the first week that was followed by a dramatic refinement after hearing onset. These changes occurred in parallel for excitatory and inhibitory input maps. However, the functional elimination of intrinsic connections was greater for excitatory than for inhibitory connections, resulting in a predominance of intrinsic inhibition after hearing onset.