Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus

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.

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

“…Recently, the precise anatomical basis of the excitatory synaptic drive of the SPON was clarified (Felix & Magnusson, ). Rather than receiving a mixed type of afferent input from the cochlear nucleus bilaterally, (Friauf & Ostwald, ; Saldaña et al., ; Schofield, ; Thompson & Thompson, ; Zook & Casseday, ), the SPON receives a predominant excitatory projection from the octopus cells in the contralateral PVCN (Felix & Magnusson, ; Felix et al., ). The octopus cells in the PVCN are broadly tuned neurons that can respond to a bandwidth of at least three octaves in vivo (Godfrey et al., ; Jiang et al., ; Palmer et al., ; Rhode & Smith, ).…”

“…This study was motivated by the recently characterized anatomical input from the octopus cells in the PVCN to the SPON in mice (Felix et al, 2017; see also Zook & Casseday, 1985;Friauf & Ostwald, 1988;Thompson & Thompson, 1991;Schofield, 1995;Saldaña et al, 2009). We hypothesized that the octopus cells could convey information about broadband transients in natural sounds to the SPON (McGinley, Liberman, Bal, & Oertel, 2012;Oertel, 2005).…”

“…Conversely, rates of BBN versus BFT spiking were not correlated for respective onset and offset responses (BBN: c = −1.6e-2, p = 0.91; BFT: c = −0.14, p = 0.4; Figure 1e), which suggests distinct mechanisms for onset and offset spiking generation. Presumably, separate input pathways that provide excitation (Felix & Magnusson, 2016;Felix et al, 2017) and inhibition (Felix et al, 2011;Kopp-Scheinpflug et al, 2011;Kuwabara, DiCaprio, & Zook, 1991) play a major role in generating onset and offset spiking.…”

“…The superior paraolivary nucleus (SPON) in the auditory brainstem is a main target of octopus cells in the contralateral PVCN (Felix et al, 2017; see also Zook & Casseday, 1985;Friauf & Ostwald, 1988; Thompson & Thompson, 1991;Schofield, 1995;Saldaña, Aparicio, Fuentes-Santamaria, & Berrebi, 2009). The SPON responds with high precision to rhythmic fluctuations of the sound envelope (Felix, Fridberger, Leijon, Berrebi, & Magnusson, 2011;Grothe, 1994;Kadner & Berrebi, 2008;Kopp-Scheinpflug et al, 2011;Kuwada & Batra, 1999).…”

Cellular Computations Underlying Detection of Gaps in Sounds and Lateralizing Sound Sources

“…They signal the presence of the onset of broadband sounds with extraordinary temporal precision [13–15], projecting to the contralateral SPON [16, 17] and to the columnar area of the VNLL [16, 18, 19] (Fig. 1A).…”