Innervation Pattern of Inhibitory Projection Neurons in the Bird Sound Localization Circuit

To navigate its environment, an animal extracts salient information from sounds using temporal and intensity cues. In birds, the nucleus laminaris (NL) detects the submillisecond differences in the arrival time of sound to the two ears, the interaural time differences (ITDs), to localize sounds. This ability is facilitated by inhibitory long-range projection neurons from the ipsilateral superior olivary nucleus (SON) that enable NL neurons to remain sensitive to ITDs across a large range of sound intensities. It is well known that the excitatory inputs to NL, from nucleus magnocellularis (NM), innervate a narrow isofrequency band along the ITD axis. However, the organization of the inhibitory input from the SON remains largely unknown. We analyzed the innervation pattern of individual axons from SON neurons within the chicken NL. SON axonal arborizations vary greatly in size and topographic organization. On average, an inhibitory SON neuron innervates one-third of both the tonotopic and ITD axes, markedly larger target regions than do the excitatory inputs from NM. Unlike the excitatory axons that are confined to one dendritic lamina (separating inputs from the two ears), most SON cells innervate both laminae to similar extents, as well as the somata of the NL neurons. In addition, we found that some NL-projecting SON neurons also send collateral axons to NM or the nucleus angularis. The pattern of synapses along SON axons suggests that the inhibitory activity of individual NL neurons is shaped by many SON neurons. A single SON neuron contributes only a small proportion of the inhibition on each NL neuron. This broad innervation pattern of SON neurons is well-suited to control the overall activity of NL, supporting accurate ITD detection in a broad range of sound environments.