Responses to oddball communication sequences in the bat frontal and auditory cortices

Abstract

Stimulus-specific adaptation (SSA) is a ubiquitous phenomenon in the animal kingdom across sensory modalities, but this type of neural response has rarely been studied using natural sounds in the auditory brain. Here, we leveraged the well-documented acoustic repertoire of the bat species Carollia perspicillata to study adaptation in the bat brain using natural communication sounds. We searched for SSA in single neuron spiking activity measured in two brain areas simultaneously: the auditory cortex and the frontal auditory field. The stimuli consisted of natural distress syllables, a form of vocalization produced by bats under duress. Bat distress vocalizations signal different degrees of urgency based on their amplitude modulation pattern, without large differences in their spectral structure. These distress vocalizations make an ideal test case for exploring the limits of neural deviance detection when considering naturalistic soundscapes with low stimulus contrast. The results show limited evidence for stimulus-specific adaptation in response to natural sound sequences in the majority of neurons studied. Many neurons did show a prominent effect related to context-dependent changes, caused by the type of sounds that occurred most frequently within each oddball sequence. Context-dependent responses were strongest in frontal neurons. Decoding analysis showed the existence of neural populations in both frontal and auditory cortices, which could distinguish between deviants and standards occurring within the same sequence, without large changes in evoked spike counts. Taken together, our results highlight the diversity of neural mechanisms complementing classical stimulus-specific adaptation when encoding natural vocalizations that do not differ markedly in their spectral composition.