Abstract
Auditory streaming enables perception and interpretation of complex acoustic environments that contain competing sound sources. At early stages of central processing, sounds are segregated into separate streams representing attributes that later merge into acoustic objects. Streaming of temporal cues is critical for perceiving vocal communication, such as human speech, but our understanding of circuits that underlie this process is lacking, particularly at subcortical levels. The superior paraolivary nucleus (SPON), a prominent group of inhibitory neurons in the mammalian brainstem, has been implicated in processing temporal information needed for the segmentation of ongoing complex sounds into discrete events. The SPON requires temporally precise and robust excitatory input(s) to convey information about the steep rise in sound amplitude that marks the onset of voiced sound elements. Unfortunately, the sources of excitation to the SPON and the impact of these inputs on the behavior of SPON neurons have yet to be resolved. Using anatomical tract tracing and immunohistochemistry, we identified octopus cells in the contralateral cochlear nucleus (CN) as the primary source of excitatory input to the SPON. Cluster analysis of miniature excitatory events also indicated that the majority of SPON neurons receive one type of excitatory input. Precise octopus cell-driven onset spiking coupled with transient offset spiking make SPON responses well-suited to signal transitions in sound energy contained in vocalizations. Targets of octopus cell projections, including the SPON, are strongly implicated in the processing of temporal sound features, which suggests a common pathway that conveys information critical for perception of complex natural sounds.
Highlights
Sensory processing relies on merging information from various stimulus features into streams, and deciphering complex sounds, such as human speech, requires delicate analysis of both spectral and temporal cues
Labeled neurons were found in the posteroventral CN (PVCN) with a clear contralateral predominance (Figure 2B), and they were readily identified as octopus cells based on their distinct dendritic shape (Figure 2C; Harrison and Irving, 1966; Saldaña et al, 1987; Pocsai et al, 2007; Bazwinsky et al, 2008)
Labeled neurons were found in inhibitory structures known to project to the superior paraolivary nucleus (SPON), including the medial and lateral nuclei of the trapezoid body (MNTB and LNTB) (Figure 2A; see Saldaña et al, 2009; Viñuela et al, 2011), as well as in the ventral tectal longitudinal column (TLCv; not shown), which may contain a mixed population of GABAergic and glutamatergic neurons (Aparicio and Saldaña, 2014)
Summary
Sensory processing relies on merging information from various stimulus features into streams, and deciphering complex sounds, such as human speech, requires delicate analysis of both spectral and temporal cues. Octopus cells in the cochlear nucleus (CN) are especially well-suited for extracting temporal information due to their broad frequency tuning (Golding et al, 1995), unsurpassed capabilities of following broadband transients (Oertel et al, 2000), and synchronous responses to amplitude-modulated (Rhode and Greenberg, 1994) and formant-like sounds (Rhode, 1998). These findings have led to the suggestion that the octopus cells extract and convey information relevant for speech segmentation (Oertel, 2005), but our understanding of how this information is processed further in the brainstem is lacking
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