Temporal information in tones, broadband noise, and natural vocalizations is conveyed by differential spiking responses in the superior paraolivary nucleus

Abstract

Communication sounds across all mammals consist of multiple frequencies repeated in sequence. The onset and offset of vocalizations are potentially important cues for recognizing distinct units, such as phonemes and syllables, which are needed to perceive meaningful communication. The superior paraolivary nucleus (SPON) in the auditory brainstem has been implicated in the processing of rhythmic sounds. Here, we compared how best frequency tones (BFTs), broadband noise (BBN), and natural mouse calls elicit onset and offset spiking in the mouse SPON. The results demonstrate that onset spiking typically occurs in response to BBN, but not BFT stimulation, while spiking at the sound offset occurs for both stimulus types. This effect of stimulus bandwidth on spiking is consistent with two of the established inputs to the SPON from the octopus cells (onset spiking) and medial nucleus of the trapezoid body (offset spiking). Natural mouse calls elicit two main spiking peaks. The first spiking peak, which is weak or absent with BFT stimulation, occurs most consistently during the call envelope, while the second spiking peak occurs at the call offset. This suggests that the combined spiking activity in the SPON elicited by vocalizations reflects the entire envelope, that is, the coarse amplitude waveform. Since the output from the SPON is purely inhibitory, it is speculated that, at the level of the inferior colliculus, the broadly tuned first peak may improve the signal-to-noise ratio of the subsequent, more call frequency-specific peak. Thus, the SPON may provide a dual inhibition mechanism for tracking phonetic boundaries in social-vocal communication.

Slow NMDA-Mediated Excitation Accelerates Offset-Response Latencies Generated via a Post-Inhibitory Rebound Mechanism

“…The relative strength and temporal interaction of excitatory and inhibitory synaptic inputs determine neuronal temporal firing patterns in many parts of the brain including the auditory pathway (Wehr and Zador, 2003; Sun et al, 2010; Denève and Machens, 2016). Acoustic pattern recognition and vocal communication require precise processing of the temporal structure of sounds, such as the distinct detection of onsets and offsets, which are encoded by two dissociable channels in the auditory pathway (Anderson and Linden, 2016; Gómez-Álvarez et al, 2018; Kopp-Scheinpflug et al, 2018).…”

Effects of age on responses of principal cells of the mouse anteroventral cochlear nucleus in quiet and noise

“…One major cell type that would be valuable to consider in future studies is octopus cells, which integrate activity from multiple ANFs tuned to different frequencies (Oertel et al, 2000). This integrative function makes them especially suited for encoding temporal information in broadband sounds, such as sound onset and offset (Golding et al, 1995), which contributes to the responses of downstream targets including the superior paraolivary nucleus (Gomez-Alvarez et al, 2018; Rajaram et al, 2019). It would be valuable to determine whether this integrative function also makes octopus cells vulnerable to loss of afferent input during aging.…”