Processing and representation of species-specific communication calls in the auditory system of bats.

Abstract Bats, perhaps more than any other animal, depend on their hearing for survival. Not only do they rely on hearing for orientation and hunting through echolocation, but hearing is also critically important for social communication. Bats live in caves where they employ a rich repertoire of spectrally and temporally complex communication calls for a wide variety of social interactions. Here we explore how their auditory systems process and represent species-specific communication calls, and derive some rules, that apply both to bats and other mammals, about how information is progressively transformed in the ascending auditory system. We first consider how complex stimuli are processed in subcortical auditory nuclei. One of the principal transformations that distinguishes the inferior colliculus (IC), the principal auditory nucleus in the midbrain, from lower nuclei is a change from processing that emphasizes similarity (homogeneity) among the neuronal population in each lower nucleus, to one that emphasizes diversity (heterogeneity) and selectivity in the IC. IC neurons are selective in that each neuron fails to respond to some, or even all calls even though those calls have energy that encroaches upon their excitatory response regions, and are heterogeneous since each IC neuron responds to a different subset of calls. The transformation from homogeneity to heterogeneity may largely be a consequence of the difference in the ways that the various excitatory and inhibitory inputs distribute along frequency contours in lower nuclei compared to the inferior colliculus. One important consequence is that those features endow the IC population with the ability to respond to any signal with a unique and pronounced spatiotemporal pattern of activity. Selectivity increases the contrast of the spatiotemporal pattern across the IC population evoked by any call. Thus instead of evoking a near continuous profile of activity across the population in each frequency contour, as occurs in lower nuclei, selectivity imposes regions of inactivity dispersed among active regions, a pattern that is then reiterated in each frequency contour. We then turn to the cortex and discuss the species specificity of cortical fields and the role of combinatorial properties in the processing of communication calls. Combinatorial neurons are prevalent in cortical regions and respond best, or only when two or more frequencies are presented with a particular temporal relationship appropriate to that neuron. Cortical neurons express combinatorial properties for both biosonar signals and for communication signals. But the most important and surprising finding is that the combinatorial properties expressed when communication signals are presented are different from the combinatorial properties that the same neurons express when biosonar signals or portions of biosonar signals are presented, suggesting that different neuronal mechanisms underlie each. Thus, there is an important role for combination sensitivity in both communication and echolocation, but combination sensitivity is far more complex than originally thought, since cortical neurons have multiple, distinct specialized modes of response for each type of signal.