Selectivity and persistent firing responses to social vocalizations in the basolateral amygdala

Abstract

This study examined responsiveness to acoustic stimuli among neurons of the basolateral amygdala. While recording from single neurons in awake mustached bats (Pteronotus parnellii), we presented a wide range of acoustic stimuli including tonal, noise, and vocal signals. While many neurons displayed phasic or sustained responses locked to effective auditory stimuli, the majority of neurons (n=58) displayed a persistent excitatory discharge that lasted well beyond stimulus duration and filled the interval between successive stimuli. Persistent firing usually began seconds (median value, 5.4 s) after the initiation of a train of repeated stimuli and lasted, in the majority of neurons, for at least 2 min after the end of the stimulus train. Auditory-responsive amygdalar neurons were generally excited by one stimulus or very few stimuli. Most neurons did not respond well to synthetic stimuli including tones, noise bursts or frequency-modulated sweeps, but instead responded only to vocal stimuli (82 of 87 neurons). Furthermore, most neurons were highly selective among vocal stimuli. On average, neurons responded to 1.7 of 15 different syllables or syllable sequences. The largest percentage of neurons responded to a hiss-like rectangular broadband noise burst (rBNB) call associated with aggressive interactions. Responsiveness to effective vocal stimuli was reduced or eliminated when the spectrotemporal features of the stimuli were altered in a subset of neurons. Chemical activation of the medial geniculate body (MG) increased both background and evoked firing. Among 39 histologically localized recording sites, we saw no evidence of topographic organization in terms of temporal response pattern, habituation, or the affect of calls to which neurons responded. Overall, these studies demonstrate that amygdalar neurons in the mustached bat show high selectivity to vocal stimuli, and suggest that persistent firing may be an important feature of amygdalar responses to social vocalizations.