Acoustic context modulates natural sound discrimination in auditory cortex through frequency specific adaptation

Vocal communication is essential to coordinate social interactions in mammals and it requires a fine discrimination of communication sounds. It is known that auditory neurons can exhibit selectivity for specific natural sounds, but how this selectivity is affected by acoustic context (i.e. other natural sounds that precede the sound in question) is still debated. Here we tackled this question by using ethologically relevant vocalizations in a highly vocal mammalian species: Seba9s short-tailed bat (Carollia perspicillata). We show that neurons in the bat auditory cortex present several degrees of selectivity for navigation (i.e. echolocation) and distress calls (a type of communication sound), ranging from exclusive selectivity to one sound category to equal responsiveness to both types of signals. Embedding vocalizations within natural acoustic streams leads to stimulus-specific suppression of neuronal responses. Such suppression changes natural sound selectivity in a disparate manner: selectivity increases in neurons that displayed poor sound discriminability in the absence of context (i.e. when sounds were preceded by silence), and decreases sound selectivity in neurons classified as selective in silent settings. A computational model indicates that the observed context-dependent effects arise from two forms of adaptation: presynaptic frequency specific adaptation acting in cortical inputs and stimulus unspecific postsynaptic adaptation. These results shed light into how acoustic context modulates natural sound discriminability in the mammalian cortex.