Two distinct representations of social vocalizations in the basolateral amygdala

Acoustic communication signals carry information related to the types of social interactions by means of their "acoustic context," the sequencing and temporal emission pattern of vocalizations. Here we describe responses to natural vocal sequences in adult big brown bats (Eptesicus fuscus). We first assessed how vocal sequences modify the internal affective state of a listener (via heart rate). The heart rate of listening bats was differentially modulated by vocal sequences, showing significantly greater elevation in response to moderately aggressive sequences than appeasement or neutral sequences. Next, we characterized single-neuron responses in the basolateral amygdala (BLA) of awake, restrained bats to isolated syllables and vocal sequences. Two populations of neurons distinguished by background firing rates also differed in acoustic stimulus selectivity. Low-background neurons (<1 spike/s) were highly selective, responding on average to one tested stimulus. These may participate in a sparse code of vocal stimuli, in which each neuron responds to one or a few stimuli and the population responds to the range of vocalizations across behavioral contexts. Neurons with higher background rates (≥1 spike/s) responded broadly to tested stimuli and better represented the timing of syllables within sequences. We found that spike timing information improved the ability of these neurons to discriminate among vocal sequences and among the behavioral contexts associated with sequences compared with a rate code alone. These findings demonstrate that the BLA contains multiple robust representations of vocal stimuli that can provide the basis for emotional/physiological responses to these stimuli.