Inputs to combination-sensitive neurons of the inferior colliculus

In the mustached bat, combination-sensitive neurons display integrative responses to combinations of acoustic elements in biosonar or social vocalizations. One type of combination-sensitive neuron responds to multiple harmonics of the frequency-modulated (FM) components in the sonar pulse and echo of the bat. These neurons, termed FM-FM neurons, are sensitive to the pulse-echo delay and may encode the distance of sonar targets. FM-FM neurons are common in high-frequency regions of the central nucleus of the inferior colliculus (ICC) and may be created there. If so, they must receive low-frequency inputs in addition to the expected high-frequency inputs. We placed single deposits of a tracer at FM-FM recording sites in the ICC and then analyzed retrograde labeling in the brainstem and midbrain. We were particularly interested in labeling patterns suggestive of low-frequency input to these FM-FM neurons. In most nuclei containing labeled cells, there was a single focus of labeling in regions thought to be responsive to high-frequency sounds. More complex labeling patterns were observed in three nuclei. In the anteroventral cochlear nucleus, labeling in the anterior and marginal cell divisions occurred in regions thought to respond to low-frequency sounds. This labeling comprised 6% of total brainstem labeled cells. Labeling in the intermediate nucleus of the lateral lemniscus and the magnocellular part of the ventral nucleus of the lateral lemniscus together comprised nearly 40% of all labeled cells. In both nuclei, multiple foci of labeling occurred. These different foci may represent groups of cells tuned to different frequency bands. Thus, one or more of these three nuclei may provide low-frequency input to high-frequency-sensitive cells in the ICC, creating FM-FM responses. We also examined whether ICC neurons responsive to lower frequencies project to high-frequency-sensitive ICC regions; only 0.15% of labeling originated from these lower frequency representations. If the spectral integration of FM-FM neurons is created at the level of the ICC, these results suggest that neurons of the anteroventral cochlear nucleus or monaural nuclei of the lateral lemniscus may provide the essential low-frequency input. In contrast, there is little evidence that the low-frequency representation of the ICC contributes to these integrative responses.