Show Summary Details

Page of

PRINTED FROM OXFORD HANDBOOKS ONLINE (www.oxfordhandbooks.com). © Oxford University Press, 2018. All Rights Reserved. Under the terms of the licence agreement, an individual user may print out a PDF of a single chapter of a title in Oxford Handbooks Online for personal use (for details see Privacy Policy and Legal Notice).

date: 13 December 2018

The Superior Paraolivary Nucleus

Abstract and Keywords

This chapter summarizes the current concepts of the superior paraolivary nucleus (SPON)—a structure embedded in the superior olivary complex in the mammalian auditory brainstem. SPON is driven by input pathways from two of the most temporally secure neurons in the brain: the octopus cells in the cochlear nucleus and the neurons of the medial nucleus of the trapezoid body. These inputs activate spiking activity that marks the onset and offset of sound, the latter based on a rebound depolarization mechanism. This makes the SPON an excellent detector of transient sound energy. A robust detection of the coarse sound pattern over time further gives SPON the capacity to track the temporal envelope of complex sounds with supreme precision. Since the SPON circuitry is constant in mammals and resilient to sensory perturbation, it indicates its high survival value. A possible neuroevolutionary role of SPON in processing of vocalizations is discussed.

Keywords: brainstem, auditory pathways, temporal processing, rebound spiking, feature detection, segmentation, prosodic stress pattern

The SPON Is Present in All Mammals

The superior olivary complex (SOC) comprises a group of morphologically-defined nuclei in the ventral brainstem. Within the SOC, the superior paraolivary nucleus (SPON) is a prominent GABAergic nucleus (González-Hernández, Mantolán-Sarmiento, González-González, & Pérez-González, 1996; Kulesza & Berrebi, 2000), which has been implicated in processing rhythmic sound cues of importance for the perception of vocalized communication (Felix et al., 2011; Kadner & Berrebi, 2008; Kopp-Scheinpflug et al., 2011). Perceiving sound rhythms is especially important in humans, who rely on the ability to identify distinct speech units for language perception (Rosen, 1992) and speech production (Lieberman, 2002). Compared to other SOC nuclei, which are well-known for their role in deriving sound localization cues (McAlpine, 2005; Tollin, 2003) or as a model for studying the developmental organization of the auditory pathways (Kandler et al., 2009; Sanes & Friauf, 2000), the SPON has received relatively little attention. This chapter summarizes recent progress in understanding the role of the SPON for hearing, and its implications for interspecies communication.

Based on cyto-architecture, the SPON (sometimes also referred to as the SPN) is a well-defined auditory brainstem nucleus in lower mammals, such as mice (Felix et al., 2011; Kopp-Scheinpflug et al., 2011; Leijon et al., 2016), rats (Kulesza & Berrebi, 2000; Caminos et al., 2007), gerbils (Behrend et al., 2002; Dehmel et al., 2002; Stange et al., 2013), and guinea-pigs (Schofield, 1991; Schofield & Cant, 1991; 1992). In other species, cells located dorsomedially of the medial superior olive (MSO), referred to as the dorsomedial periolivary nucleus (DMPO), are commonly speculated to be the SPON homologue in, for example, bats (Grothe, 1994; Zook & Casseday, 1985;), cats (Adams, 1983; Spirou et al., 1990), chinchillas (Azeredo et al., 1999; Kelley et al., 1992), and primates (Bazwinsky et al., 2005; Moore & Moore, 1971; Strominger et al., 1977), including humans (Bazwinsky et al., 2003; Moore et al., 1998; Moore, 2000). Although studies to systematically characterize the physiological properties of DMPO in vivo are largely missing in the mustached bat, the medial SOC exhibit SPON-like properties in response to monaural sound stimulation (Grothe et al., 1994; Kulesza et al., 2003), thus showing it as being homologous to the rodent SPON (Grothe, 2000). Recently, the nomenclature in humans has shifted from the DMPO to the SPON (Kulesza, 2008, 2014; Kulesza & Grothe, 2015; Schmidt et al., 2010).

The Superior Paraolivary NucleusClick to view larger

Figure 1 Schematic representation of the superior olivary complex in humans, cats, bats, and rats. The lateral (LSO) and the medial superior olivary nuclei (MSO) vary in size depending on the animal’s natural acoustic niche (Heffner, 2004), whereas the superior paraolivary nucleus (SPON) and the medial nucleus of the trapezoid body (MNTB) are more uniformly represented throughout the animal chain. The nuclear structures are based on transverse brainstem sections and are inspired from, for example, Moore (2000); Zook & Casseday (1985).

Numerous anatomical investigations of the SOC reveal that the SPON/DMPO is present in all mammals investigated thus far (see Figure 1). An inspection of the nuclear morphology in SOC brain sections containing the MSO, SPON/DMPO and medial nucleus of the trapezoid body (MNTB; Figure 1) demonstrate that these areas expand proportionally in line with the increase in brainstem size from small rodents to primates, including humans (Figure 1; Kulesza, 2008, 2014; Moore, 1987, 2000; Moore et al., 1998). The size of the SPON/DMPO (Moore & Moore, 1971), however, does not depend on the animals hearing range (Heffner, 2004). Thus, the SPON is a major part of the SOC in animals in which high frequency hearing dominates, such as mice and rats (Kulesza et al., 2002), as well as those in which low frequency hearing is more prominent, such as gerbils (Behrend et al., 2002; Dehmel et al., 2002; Stange et al., 2013) and guinea-pigs (Schofield, 1991; Schofield & Cant, 1991, 1992). Accordingly, species that capitalize on both high and low sound frequency cues, such as the cat (Heffner, 2004), exhibit a balanced ratio between the LSO, MSO and DMPO (Figure 1; Moore, 2000). The naked mole rat is a special case since it is most sensitive to very low frequency sounds (<1 kHz; Lange et al., 2007), which may lead to an expansion of the SPON at the expense of the high frequency-sensitive LSO, a hypothesis that needs to be verified by identifying the SPON neurons using, for example, GABA markers.

The SPON Receives Monaural Temporal Information

In rodents, one set of afferents to the SPON come from a mixed population of octopus and multipolar stellate cells in the contralateral posteroventral cochlear nucleus (PVCN; Friauf & Ostwald, 1988; Saldaña et al., 2009; Schofield, 1995; Thompson & Thompson, 1991; Zook & Casseday, 1985). The multipolar stellate cell type has also been described as forming an ipsilateral projection from the PVCN to the SPON (Friauf & Ostwald, 1988). Recently, this view was challenged by Felix et al. (2017), who demonstrated that a focal injection of a retrograde tracer in the SPON of mice only labeled the octopus cells in the contralateral PVCN (see Figure 2), whereas virtually no multipolar stellate cells were labeled in either the ipsilateral or contralateral PVCN. No tracer was observed in the ventral acoustic stria or in the anteroventral cochlear nucleus (Felix et al., 2017). The latter result confirms previous studies in SPON of rodents (Friauf & Ostwald, 1988; Kuwabara et al., 1991), whereas in the cat there is conflicting evidence for a globular bushy cell projection from the contralateral anterior ventral cochlear nucleus (AVCN). to the DMPO (Smith et al., 1991; Spirou et al., 1990). However, the slightest spread of tracer into adjacent areas of the SOC targets globular bushy cells and multipolar stellate cells in, respectively, AVCN and PVCN on both sides of the brainstem (Felix et al., 2017). Therefore, the most parsimonious interpretation is that SPON receives a single input from the octopus cells located in the contralateral PVCN (Figure 2; Felix et al., 2017). A statistical analysis of miniature excitatory currents (mEPSCs) recorded and pharmacologically isolated in the SPON and LSO neurons lends further support to the concept of a single input to the principal neurons of these nuclei. In contrast, the lateral olivocochlear neurons, also residing in the LSO (Aschoff & Ostwald, 1987; Motts et al., 2008), but with distinct morphological and physiological properties from the principal neurons (Adam et al., 1999; Fujino et al., 1997; Leijon & Magnusson, 2014; Sterenborg et al., 2010), displayed evidence for two or more inputs (Felix et al., 2017; Gómez-Álvarez & Saldaña, 2016). Recordings from the SPON in vivo show that sound primarily actives the SPON from the contralateral ear (bat: Grothe et al., 1994; rabbit: Kuwada & Batra, 1999; gerbil: Behrend et al., 2002; Dehmel et al., 2002; rat: Kadner & Berrebi, 2008; Kulesza et al., 2003, 2007; mouse: Felix et al., 2011; Kopp-Scheinpflug et al., 2011), although there have been reports of some responses, putatively from SPON neurons, that are binaural (Behrend et al., 2002; Dehmel et al., 2002). A monaural activation of the SPON, driven by octopus cells, is consistent with the hypothesis that the SPON extracts temporal information induced by broadband sounds (Felix et al., 2013, 2017; Oertel et al., 2000; Rhode, 1998).

The Superior Paraolivary NucleusClick to view larger

Figure 2 The superior paraolivary nucleus (SPON) connectome. The SPON receives direct excitatory input from the octopus cells in the contralateral posteroventral cochlear nucleus (PVCN), via the intermediate acoustic stria (Felix et al., 2017), and an indirect inhibitory glycinergic input from the medial nucleus of the trapezoid body (MNTB) via the globular bushy cells (GBCs) in the contralateral anteroventral cochlear nucleus (AVCN). The ipsilateral lateral nucleus of the trapezoid body (LNTB) provides an additional source of glycinergic inhibition of unknown function via GBCs in the ipsilateral AVCN. The SPON projects tonotopically to the ipsilateral inferior colliculus (IC) via the nuclei of the lateral lemniscus (NLL) (Saldaña et al., 2009; Viñuela et al., 2011). The SPON also projects to the ipsilateral and, to a lesser degree, to the contralateral tectal longitudinal column (TLC), the periaqueductal gray substance (PAG), and the deep layers of the contralateral superior colliculus (SC) in the midbrain tectum (Viñuela et al., 2011).

Another documented major projection to the SPON is from the ipsilateral principal neurons in the medial nucleus of the trapezoid body (MNTB; Figure 2; Banks & Smith, 1992; Bledsoe et al., 1990; Ford et al., 2009; Kuwabara & Zook, 1991; 1992; Sommer et al., 1993; Spangler et al., 1985; Warr, 1966). The MNTB neurons receive input from the globular bushy cells in the contralateral AVCN, the axons of which travel in the ventral acoustic stria and terminate with the calyx-of-Held endings onto the MNTB principal neurons (Kuwabara et al. 1991; Smith et al. 1991; Spirou et al., 1990). The MNTB-projection to the SPON gives rise to a powerful feed-forward glycinergic inhibition that quench SPON activity during contralateral sound stimulation but, paradoxically, drives the neurons to spike at the sound offset (Kadner et al., 2006; Kulesza et al., 2007). Interestingly, a single afferent from the MNTB can branch and innervate several nuclei within the SOC (Kuwabara & Zook, 1991, 1992; Gómez-Álvarez & Saldaña, 2016; Sommer et al., 1993). It is not clear how these afferent collaterals from the MNTB contribute to sound processing in areas fulfilling vastly different roles for acoustic processing. Presumably, neuron-specific properties, such as voltage-operated mechanisms (Felix et al. 2011, 2013;Kopp-Scheinpflug et al., 2011, 2015; Yassin et al., 2014), enable the SPON, perhaps in combination with the termination pattern in relation to the cellular geometry (Felix et al., 2013; Ollo & Schwartz, 1979), to decode specific aspects of the incoming signals. In addition, the SPON receives projections from the ipsilateral lateral nucleus of the trapezoid body (LNTB; Figure 2; Felix et al., 2017; Saldaña et al., 2009; Viñuela et al., 2011). The LNTB is innervated by ipsilateral collateral branches of the globular bushy cell axons, (Kuwabara et al. 1991; Spirou et al. 1990), thus providing the SPON with an ipsilateral inhibitory glycinergic (Magnusson et al., 2005; Roberts et al., 2014) projection of hitherto unknown function.

The SPON Relays Temporally Precise Inhibition

The main output from the SPON is a tonotopically organized inhibitory, GABAergic projection to the ipsilateral inferior colliculus (IC) via the nuclei of the lateral lemniscus (NLL; see Figure 2; Saldaña et al., 2009; Viñuela et al., 2011). The function of such tonotopic GABA-ergic drive from the SPON was recently tested by performing paired recordings from the SPON and the IC, which demonstrated that the selective blockade of SPON-derived inhibition decreased IC spiking precision in response to the envelope of amplitude-modulated sounds (Felix et al., 2015). This fit well with the envelope-synchronized spiking response to amplitude-modulated sounds recorded in SPON (Behrend et al. 2002; Felix et al., 2011; Grothe, et al., 1994; Kadner & Berrebi, 2008; Kulesza et al., 2003; Kuwada & Batra, 1999). The inhibitory output from the SPON would, therefore, be suitable to tune the IC neurons to sound envelope cues (Barsz, et al., 1998; Krishna & Semple, 2000; Zheng & Escabí, 2008) and periodicity patterns, that is, how often these coarse fluctuations occur (Langner, 1992; Rees & Palmer, 1989; Schreiner & Langner, 1988). It is tempting to speculate that the topographical representation of sound periodicity, visualized by functional magnetic resonance imaging (fMRI) on the IC level (Baumann et al., 2011), may depend on inhibition from lower brainstem areas, such as the input from SPON. A shift in sensitivity from high to low modulation-frequencies in the ascending auditory pathways, from the cochlear nucleus to the IC (Frisina, 2001; Joris et al., 2004; Nelson & Carney, 2004), suggests that the auditory brainstem would be a suitable locus to perform the conversion needed to give rise to the IC periodicity map. The SPON is a suitable candidate for changing the coding strategy. Because rebound spiking in SPON neurons depends on the activation of slowly activating h-currents (Felix et al., 2011; Kopp-Scheinpflug et al., 2011), offset spiking to sound depends on relatively long-lasting MNTB activity, which results in temporal summation of the hyperpolarizing inputs (Felix et al., 2011). By acting as a low-pass filter, Ih-dependent rebound spiking in SPON would be well suited to encode slow changes in sound energy over time as it typically occurs in periodic natural sounds, such as speech (Rosen, 1992; Shannon et al., 1995). By providing robust inhibition, synchronized to the negative edge of sound segments, SPON may not only help to enhance the “peaks” of the envelope signal by unmasking excitation (Grothe et al., 1994; Yang & Pollak, 1997) or phasic disinhibition of inhibitory interneurons in the IC (Malmierca et al., 2009; Oliver & Morest, 1984), but could also trigger rebound spiking in the IC (Koch & Grothe, 2003; Tan et al., 2007; Sun & Wu, 2008; Nagtegaal & Borst, 2010). The slightly delayed SPON input could, therefore, contribute to further lowering the preferred modulation frequency of the neurons in the IC (Langner, 1992; Rees & Palmer, 1989; Schreiner & Langner, 1988), while inverting the sign of the auditory signal from excitation to inhibition in SPON would enhance the modulation depth of the IC envelope-response at both the “peaks” and the “troughs” (Felix et al., 2015). The “troughs” could, according to de Cheveigné’s cancellation model for pitch perception (1998), equally well serve as a periodicity cue as the “peaks.” Another suggested role for SPON-derived inhibition is related to post-stimulus inhibition, which produces a forward masking effect in the IC (Nelson et al., 2009; Salimi et al., 2017). This mechanism could further enhance the contrast between sound units and aid perception of communication sounds.

Ascending SPON axons continue from the ipsilateral IC and travel through the commissure of the IC (CoIC) before terminating in the tectal longitudinal column (TLC). The newly discovered TLC is a distinct group of reticular neurons spanning the midbrain tectum longitudinally, very close to the midline and immediately above the periaqueductal gray (PAG; Figure 2; Aparicio et al., 2010; Aparicio & Saldaña, 2014; Marshall et al., 2008; Saldaña et al., 2007, 2009; Viñuela et al., 2011). The SPON projects densely to the ipsilateral TLC, and sparsely to the contralateral TLC (Saldaña et al., 2009; Viñuela et al., 2011). A small fraction of the ascending SPON axons circumvent the IC and cross to innervate the deep layers of the contralateral superior colliculus (SC) and the PAG (Figure 2; Viñuela et al., 2011), which are multimodal areas expected to trigger automated motor actions in response to external and internal signals of importance for the organism’s survival (Holstege, 1998; Sparks & Hartwich-Young, 1989). Notably, injections of pseudorabies virus in the rabbit eyelid has recently demonstrated tentative evidence for a projection from the SPON to the superior salivatory nucleus (SSN; Wang et al., 2017). The SSN is a group of parasympathetic neurons that innervate the lacrimal, sublingual and submandibular glands (Tóth et al., 1999). Although a connection between the SPON and areas involved in autonomic regulation still has to be confirmed, it is tempting to speculate that the SPON, with its high sensitivity to the sound envelope (Behrend et al., 2002; Felix et al., 2011; Kadner & Berrebi, 2008; Kulesza et al., 2003; Kuwada & Batra, 1999), may be part of an old gateway mediating innate reactions to sounds, for instance, in response to the affective qualities of the voice (Pihan et al., 2008).

The SPON Receives Descending Projections but Is Most Likely Not a Major Part of the Medial Olivocochlear Efferent System

The SPON has long been considered to be a subdivision of the medial olivocochlear efferent system projecting from the brainstem to the cochlear nucleus and the cochlea. This concept builds mostly on anatomical studies performed in cats (Adams & Warr, 1976; Smith et al., 1991; Warr, 1975; Warr et al., 2002), but also studies in chinchillas (Azeredo et al., 1999), guinea-pig (Winter et al., 1989), mice (Ollo & Schwartz, 1979), and bats and rats (Aschoff & Ostwald, 1987). A close, specific, examination of the periolivary cells in the cat demonstrated that the ventromedial part of the SOC, including the SPON, the MNTB and the ventral nucleus of the trapezoid body (VNTB), are indeed targeted by the retrograde transporter HRP injected in the cochlea (Adams, 1983). However, the SPON was also targeted by HRP-injections into the ipsilateral IC. These IC retrogradely labeled neurons far outnumbered those that projected back to the cochlear nucleus or cochlea and importantly, were other neurons than the efferent ones (Adams, 1983; Adams & Warr, 1976). Instead, the majority of the cochlear-projecting neurons were confined to the VNTB (Adams, 1983). This result is consistent with other species that demonstrate that cholinergic neurons, known to be the main neurotransmitter of the olivocochlear system (Simmons, 2002), are predominantly located within the LSO and the VNTB (human: Moore et al., 1999; monkey: Thompson & Thompson, 1986; guinea-pig: Motts et al., 2008; gerbil: Kaiser et al., 2011; hamster: Simmons et al., 1999; rat; Yao & Godfrey, 1998; mouse: Brown & Levine, 2008; Leijon & Magnusson, 2014). In a rat study that traced the inputs from the SOC to the cochlea, only neurons in the LSO and the VNTB were highlighted; thus, White & Warr (1983) concluded that the VNTB is the only periolivary nucleus that has been invariably targeted by anatomical tract tracing of the olivocochlear efferent system in all species studied thus far.

Corticofugal projections primarily target the VNTB (Coomes, Peterson, & Schofield, 2007; Coomes & Schofield, 2004; Feliciano et al., 1995; Mulders & Robertson, 2000), and more rarely the SPON/DMPO (Coomes & Schofield, 2004; Coomes Peterson & Schofield, 2007; Feliciano et al., 1995); however, more extensive descending cortical input to the SPON has been described in the gerbil (Budinger et al., 2000; 2013). A study combining tracer injections into the cortex and the IC revealed that corticofugal fibers predominantly connect to the ipsilateral SPON neurons projecting to the ipsilateral IC, and to a lesser degree the contralateral SPON neurons that project to the ipsilateral IC (Coomes Peterson & Schofield, 2007). The ipsilateral IC is, in itself, a source of descending input to the SPON (see Figure 2; Caicedo & Herbert, 1993; Vetter et al., 1993), indicating that there is reciprocal contact between the SPON and its ascending targets. In analogy with this notion, the SPON is reciprocally connected to the ipsilateral TLC (Figure 2; Viñuela et al., 2011; Aparicio & Saldaña, 2014). It is also worth mentioning that there is a thalamic input to the SPON, consisting of a bilateral projection from the subparafascicular nucleus (SPF) with an ipsilateral dominance (Yasui et al., 1992). The SPF is, like the auditory cortex, also reciprocally connected with the external layers of the IC (LeDoux et al., 1985). The external IC region (shell region) is involved in adaptive processes that participate in the alignment of the external representation of the environment (Gutfreund & Knudsen, 2006; Knudsen & Konishi, 1978) based on its multiple sensory inputs (Jain & Shore, 2006). A strong feedback arising from such extralemniscal pathways, via the SPF to the SPON, implies that the ascending relay of auditory information routed via the SPON may be modulated in a “top-down” manner.

Rebound Spiking Enables a High Fidelity Response to Sound Rhythms in SPON Neurons

SPON activity is characteristically triggered at the cessation of contralateral sound stimulation, resulting in an offset response (see Figure 3A), which has been documented in vivo in all mammals studied so far (bat: Grothe et al., 1994; rabbit: Kuwada & Batra, 1999; gerbil: Behrend et al., 2002; Dehmel et al., 2002; rat: Kadner & Berrebi, 2008; Kulesza et al., 2003; 2007; mouse: Felix et al., 2011; 2013; Kopp-Scheinpflug et al., 2011). In addition, the SPON exhibits well-timed transient spiking at the sound onset (Figure 3A; Behrend et al., 2002; Dehmel et al., 2002; Grothe et al., 1994; Felix et al., 2013, 2015; Kulesza et al., 2003; Kuwada & Batra, 1999). This typical on-off spiking behaviordriven by, respectively, the temporally specialized octopus (Golding et al., 1999) and the MNTB neurons (Klug & Trussell, 2006) has been speculated to convey information about the coarse temporal sound structure. Periodicity patterns, such as abrupt changes in sound energy (Kadner & Berrebi, 2008; Kulesza et al., 2003), silent gaps in ongoing sounds (Kopp-Scheinpflug et al., 2011), or the temporal envelope of sounds (Felix et al., 2011; 2013; Grothe et al., 1994; Kuwada & Batra, 1999), are examples of cues that would be compatible with the response properties of the SPON. In line with the notion that the SPON is suited to faithfully transmission sound rhythms, the SPON neurons fire with high precision in synchrony with more temporally complex stimuli than tones (see Figure 3B). For instance, the SPON phase-locks extremely well to the envelope of sinusoidally amplitude-modulated sounds (Figure 3B; Behrend et al. 2002; Felix et al., 2011, 2013; Kadner & Berrebi, 2008; Kulesza et al., 2003; Kuwada & Batra, 1999), implying that the on-off-spiking (Figure 3A) is acting in tandem to ensure precise spiking with the upstroke of the signal (Figure 3B).

The Superior Paraolivary NucleusClick to view larger

Figure 3 Electrophysiological responses of superior paraolivary nucleus (SPON) neurons. (A) The typical SPON neuron response recorded in an anesthetized animal, elicited by a pure tone at the neuron’s best frequency, that is, at 3 kHz, and presented at the contralateral ear, characteristically triggers spiking at the onset and at the offset of the sound. Note that there is no spiking during the actual tone presentation, since the SPON is inhibited by its medial nucleus of the trapezoid body (MNTB) input. The preceding onset response is elicited by excitation from the octopus cells. (B) Presentation of a sinusoidal amplitude modulation of the 3 kHz pure tone produces spiking activity, which phase-locks to the envelope of the modulated tone. (C) The underlying cellular mechanism for the sound-evoked offset response in the SPON neuron (A) builds upon the membrane potential rebounding to more depolarized levels at the cessation of a hyperpolarization. When the rebound depolarization reaches the spike threshold, action potentials are elicited. Rebound spiking is abolished by applying the T-type calcium channel blocker Mibefradil and the HCN-channel blocker ZD7288, verifying that these two voltage-operated cation channels act in tandem to cause the rebound depolarization. (D) Three SPON response types are found based on the firing pattern triggered by depolarizing intracellular current steps in vitro. Onset neurons typically only fire one or a few spikes, while adapting and burst neurons fire multiple spikes, the latter with an initial burst of spikelets.

Figures are adapted from Felix et al. (2011, 2013).

The SPON’s spiking response is suppressed during the sound presentation (Figure 3A; Kulesza et al., 2003), due to the fact that the SPON is subjected to powerful glycinergic inhibition when activated by tone stimulation at the contralateral ear (Kulesza et al., 2007; Kuwabara et al., 1991). Pharmacological blockade of glycine receptors in the SPON has confirmed that the inhibitory drive from the MNTB is essential for generating the transient offset spiking response (Kulesza et al., 2007). The cellular mechanism underlying the offset response in vivo has been causally linked to rebound spiking by studying SPON neurons in vitro (Felix et al., 2011; Kopp-Scheinpflug et al., 2011). Rebound spiking occurs when the membrane potential depolarizes abruptly after hyperpolarization (Aizenman & Linden, 1999) for instance, caused by glycine receptor activation (Kopp-Scheinpflug et al., 2011). In SPON neurons, the rebound depolarization builds upon activation of two voltage-dependent currents: the non-selective cation h-current (Ih) and the low voltage activated calcium current of T-type (see Figure 3D; Felix et al., 2011; Kopp-Scheinpflug et al., 2011). The Ih is partially activated at the resting membrane potential, but activates fully at more negative voltages with a V1/2 around –90 mV in SPON (Felix et al., 2011; Kopp-Scheinpflug et al., 2011). The depolarizing effect of the Ih on the membrane potential is manifested as a “voltage-sag” when a hyperpolarizing current is injected into the neurons (see Figure 3C; Felix et al., 2011; Kopp-Scheinpflug et al., 2011), as previously demonstrated in auditory brainstem neurons (Koch & Grothe, 2003; Nagtegaal & Borst, 2010; Tan et al., 2007; Sun & Wu, 2008). The non-inactivating property of the Ih (Robinson & Siegelbaum, 2003) rapidly depolarizes the neuron upon release from hyperpolarization, which can exceed action potential threshold, leading to a Na+-spike (Figure 3D; Felix et al., 2011; Kopp-Scheinpflug et al., 2011). This rebound spiking mechanism depends on both the duration and strength of the preceding hyperpolarization (inhibition) in SPON neurons (Felix et al. 2011; Kopp-Scheinpflug et al., 2011). Inhibition-driven hyperpolarization in the SPON neuron is enhanced by an extraordinarily low (~ –100 mV) chloride reversal potential (Löhrke et al. 2005; Kopp-Scheinpflug et al., 2011). Another mechanism that enables the rebound depolarization to reach spike threshold is the T-type calcium current (Figure 3C; Felix et al., 2011; Kopp-Scheinpflug et al., 2011). Due to its activation properties (Pérez-Reyes, 2003), the T-type calcium current operates in a limited voltage range and depends on intermittent hyperpolarizations for its deinactivation (McCormick & Huguenard, 1992). Periodic influx of calcium through T-type channels may underlie network-related theta oscillations (Dickson et al., 2000; Fisahn et al., 2002; Pape & McCormick, 1989; Strohmann et al., 1994) or rhythmic pacemaker activity (Park et al., 2010; Steriade et al., 1993) in neurons. A subclass of SPON neurons located in its dorsolateral quadrant show complex rebound spiking driven by T-type currents (Felix et al., 2011, 2013; Kopp-Scheinpflug et al., 2011; Leijon et al., 2016). SPON neurons responding in vitro with single versus complex spiking at the rebound are likely to relate to the offset-response types: offset transient and offset-chopper, documented in vivo (Kulesza et al., 2003). The functional significance of a calcium-dependent, robust, but temporally less defined offset spiking response in a subset of SPON neurons remains to be explored. Importantly, rebound spiking has been unequivocally linked to SPON’s physiological response to sounds in living animals. Blocking the Ih and the T- type calcium current with specific antagonists ZD7288 and Mibefradil, while simultaneously presenting a tone at the contra-ear, invariably abolishes offset spiking in SPON in a reversible manner (Figure 3A, C; Felix et al., 2011).

The SPON Develops Properties Compatible with Precise Spiking

The developmental plasticity of SOC neurons and their inputs are well investigated (reviewed elsewhere: e.g., Hoffpauir et al. 2009; Kandler et al, 2009). Although earlier studies have demonstrated that SPON neurons are subjected to early postnatal developmental plasticity (Caicedo et al., 1998; Friauf, 2000; Friauf et al., 1999; Kandler & Friauf, 1995; Löhrke et al., 2005), it is only recently that we have begun to understand the development of the SPON’s cellular properties, mostly as a result of intracellular patch-clamp recordings in acute brain slices in mice. The period of hearing onset, which occurs at P10–P12 in mice (Mikaelian & Ruben 1965), is commonly used to demark the period around which developmental plasticity occurs in the SPON (Felix et al., 2011; Felix & Magnusson, 2016; Leijon et al., 2016). The most important finding is that the membrane time constant of SPON neurons decreases to a value of around ~3ms during the weeks surrounding hearing onset (Felix et al., 2013). This intrinsic membrane property is related to a strong up-regulation of the Ih in SPON neurons (Leijon et al., 2016). Since the Ih is constitutively active in SPON neurons at the resting membrane potential, it lowers the membrane time constant which supports fast processing of the synaptic inputs (Felix & Magnusson, 2016). SPON neurons share the fast integrative property with other SOC neurons (Chirila et al. 2007; Hassfurth et al., 2009); Kandler & Friauf 1995; Magnusson et al. 2005; Sanes 1993; Scott et al. 2005, , thus emphasizing the importance of the SOC for preserving temporal information. A fast membrane time constant also promotes brief action potentials (~1ms) in the SPON (Felix et al., 2013), providing further support for the idea that the SPON is specialized for extracting and relaying information about transient events by integrating synaptic input from temporally specialized pathways, that is, the octopus cell (Felix et al., 2017) and the MNTB pathway (Kuwabara et al., 1991).

The developmental aspects of the excitatory input to SPON were recently explored by stimulating the fibers of the intermediate acoustic stria around hearing onset in brainstem slices from mice (Felix & Magnusson, 2016). By comparing the ratio of minimal and maximal stimulation of the input fibers, it was shown that the SPON receives few excitatory input fibers, albeit with high release probability, throughout the postnatal maturation of the auditory brainstem (Felix & Magnusson, 2016). A strong, all-or-nothing excitation in SPON neurons is consistent with one type of excitatory input (Felix & Magnusson, 2016), giving rise to a well-defined onset response to sounds in vivo (Grothe et al., 1994; Behrend et al., 2002; Dehmel et al., 2002; Kulesza et al., 2003; Kuwada & Batra, 1999; Felix et al., 2013). It is worth mentioning here that when the SPON is subjected to depolarizing steps, equivalent to strong supra-threshold excitation, the corresponding firing pattern clearly reveals three response groups: onset spiking neurons that respond with a single spike, burst spiking neurons, and adapting neurons responding with sustained spiking that is adaptive (see Figure 3D; Felix et al., 2013). Since the ratio between response groups does not change with auditory development (Felix et al., 2013), this subunit classification probably reflects the postsynaptic properties of the SPON neurons (Felix et al., 2011, 2013) rather than differential connectivity (Felix et al., 2017). In line with this notion, the dendritic morphology (Ollo & Schwartz, 1979) correlates with the response groups in the SPON neurons independently of their developmental stage (Felix et al., 2013).

The SPON Is Resilient to Sensory Deprivation

Despite a consensus regarding the importance of preserving rhythmical sound information for an optimal outcome of auditory prostheses in the deaf condition (Rauschecker & Shannon, 2002; Wilson et al., 1991), the SPON has not been investigated thoroughly in the deaf or sensory deprived condition. Recently, the influence of congenital deafness on the postnatal development of SPON was investigated (Leijon et al., 2016) in mice lacking activity in the auditory nerve due to genetic deletion of the voltage-gated L-type Ca2+ channel isoform (Platzer et al., 2000). A sequence of cellular plasticity compensated for the sensory deprivation and rescued the rebound spiking in the deaf SPON. At an early postnatal age, corresponding to pre-hearing onset in the sensory activity-deprived SPON neurons, calcium currents compensate for low Ih levels and rescue the rebound depolarization. Later, at an equivalent post-hearing onset age, hyperpolarization-activated cyclic nucleotide-gated ion (HCN)2-channels are more strongly expressed than HCN1-channels, which upregulate the Ih to normal levels comparable to the hearing SPON (Leijon et al., 2016). Presumably, the HCN2 channel subtype, being less voltage sensitive, makes the SPON neurons more excitable (Kopp-Scheinpflug et al., 2015). The stereotyped timeline of compensatory mechanisms allowing for a near normal development of rebound spiking even in absence of sensory inputs to SPON implies that the final set point of excitability may be under genetic control in these neurons. The robustness of the SPON circuitry to sensory perturbation is further illustrated by genetic ablation of its main inhibitory input from the MNTB, which surprisingly results in still normal inhibitory responses in the SPON (Altieri et al., 2014; Jalabi et al., 2013). The inhibitory input from the ipsilateral LNTB (Felix et al., 2017; Viñuela et al., 2011), could possibly be a vestigial pathway, which can serve as a replacement for inhibition in such conditions. The fact that the pathways and cellular mechanisms underlying the processing of the coarse temporal sound cues are preserved in the sensory deprived SPON could be a key aspect in the success of cochlear implants. These devices, which provide means of hearing to deaf individuals by conveying temporal envelope cues (Bacon & Viemeister, 1985) directly to the brain by electrical train stimulation of the auditory nerve—that is, providing speech rhythm cues (Rauschecker & Shannon, 2002; Wilson et al., 1991) —could hypothetically be dependent on an intact SPON circuitry.

The SPON: Early-Level Processing of Prosodic Information?

The serial nature of communicating sounds demands that the auditory system can perceive the vocalizations as single elements, preserve their temporal sequence, and simultaneously segregate them from other sounds, that is, sustained background noise (Shamma & Micheyl, 2010). Accordingly, detection of intervals in between the communicative sound elements or steep amplitude fluctuations is crucial for speech perception (Bertoncini et al., 2009; Drullman et al., 1994; Shannon et al., 1995; Smith et al., 2002). The frequency analysis performed by the cochlea is an important tool for analyzing complex sounds (Bidelman & Bhagat, 2017; Licklider, 1951), but how temporal patterns carried by the voice are singled out and preserved by neural activity in the brain is less well understood.

Mouse vocalizations are characterized by a rich repertoire of social calls (; Arriaga et al., 2012; Ehret & Bernecker, 1986; Gaub & Ehret, 2005; Grimsley et al., 2011, 2016; Liu et al., 2006, Portfors, 2007), including mouse courtship song (Holy & Guo, 2005; reviewed by Egnor & Seagraves, 2016). There are theories that the perception of communication sounds specifically builds on the mammalian auditory system’s inherent sensitivities to detect small differences or discontinuities in sound, giving rise to auditory contrasts (Kuhl, 1986). Indeed, the sensitivity to auditory contrasts in harmonically structured vocalizations coincides in humans and mice (Ehret, 2005; Ehret & Riecke, 2002; Geissler & Ehret, 2002). If such common basic-biological rules exist for the auditory processing of temporal and tonal information embedded in vocalizations, it establishes an important evolutionary connection between animal communication and human speech and language perception (Kuhl, 1986). Given that the production of innate vocalizations, such as laughter, are conserved on a midbrain level in both rats and humans (Holstege & Subramanian, 2016; Panksepp, 2007; Panksepp & Burgdorf, 2003), it is tempting to suggest that the neural substrate for auditory processing of non-syntactic communication cues, such as voice prosody recognized and used by infants to communicate with a parent (Gervain & Werker, 2013; Mampe et al., 2009; Sambeth et al., 2008), critically builds on subcortical processes that extract the sound envelope rhythm. We hypothesize that rhythmic voice modulations, a capacity rooted in the concept of proto-musicality (Bannan, 2012; Bryant, 2013; Falk, 2004; Fitch, 2006; Panksepp & Trevarthen, 2009), is at least partially extracted in the evolutionary hardwired SPON circuitry (Jalabi et al., 2013; Leijon et al., 2016; Löhrke et al., 2005). We further suggested that such tonal patterns extracted on a brainstem level (Musacchia et al., 2007) may be of importance for driving the development of language and other social communication skills in a bottom-up brain-mind maturation process (Aitken & Trevarthen, 1997; Panksepp, 2015; Panksepp & Trevarthen, 2009). Interestingly, the SPON is malformed in autistic subjects (Kulesza & Mangunay, 2008), as well as in animal models of autism (Lukose et al., 2011). Studying the SPON in autistic animal models may help us to better understand human conditions that are related to difficulties in processing rhythmic information in socially-relevant communication sounds, including centrally rooted auditory processing disorders (Bamiou et al., 2001), developmental dyslexia (Goswami, 2015) and autistic spectrum disorders (Trevarthen & Delafield-Butt, 2013).

Summary

This chapter highlights the current concepts regarding the SPON from phylogenetic, developmental, mechanistic, and functional points of view. It is speculated that the SPON, being a highly conserved nucleus across mammals, plays a role in processing vocalizations and other natural sounds by decoding sound rhythms and other temporal patterns. To better understand the hierarchically structured abilities to use sound rhythms for interspecies communication, including human speech, it is important to reveal the basic biological processes in animal models, which reduce the level of communicative complexity. Knowledge gained from studying how the brain analyzes the acoustic aspects of voiced communication in animal models will eventually help us to understand various human communication disorders that are rooted in temporal processing deficits or affective-emotional communicative dysfunctions, such as autism. The genetic basis underlying variations in sensory processing is only in its infancy. More nuanced animal models of communication disorders, for instance, taking into account the level of speaking fluency, or mice with communication learning disabilities, applied together with behavioral perception tasks, provide a tantalizing prospect of shedding light on the biology of spoken language in all its forms.

Dedicated to the late Jaak Panksepp—a great scholar and friend

Acknowledgments

This chapter was written during a scholarship from The Consejo Nacional de Ciencia y Tecnología—CONACYT (M. Gómez-Álvarez; grant 665699).

References

Adam, T. J., Schwartz, D. W., & Finlayson, P. G. (1999). Firing properties of chopper and delay neurons in the lateral superior olive of the rat. Experimental Brain Research 124(4), 489–502.Find this resource:

Adams, J. C. (1983). Cytology of periolivary cells and the organization of their projections in the cat. Journal of Comparative Neurology 215(3), 275–289.Find this resource:

Adams, J. C., & Warr, W. B. (1976). Origins of axons in the cat’s acoustic striae determined by injection of horseradish peroxidase into severed tracts. Journal of Comparative Neurology 170(1), 107–121.Find this resource:

Aitken, K. J., & Trevarthen, C. (1997). Self/other organization in human psychological development. Development and Psychopathology 9(4), 653–677.Find this resource:

Aizenman, C. D., & Linden, D. J. (1999). Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. Journal of Neurophysiology 82(4), 1697–1709.Find this resource:

Altieri, S. C., Zhao, T., Jalabi, W., & Maricich, S. M. (2014). Development of glycinergic innervation to the murine LSO and SPN in the presence and absence of the MNTB. Frontiers in Neural Circuits 8, 109.Find this resource:

Aparicio, M. A., & Saldaña, E. (2014). The dorsal tectal longitudinal column (TLCd): A second longitudinal column in the paramedian region of the midbrain tectum. Brain Structure and Function 219(2), 607–630.Find this resource:

Aparicio, M. A., Viñuela, A., & Saldaña, E. (2010). Projections from the inferior colliculus to the tectal longitudinal column in the rat. Neuroscience 166(2), 653–664.Find this resource:

Arriaga, G., Zhou, E. P., & Jarvis, E. D. (2012). Of mice, birds, and men: The mouse ultrasonic song system has some features similar to humans and song-learning birds. PloS One 264(1), 56–72.Find this resource:

Aschoff, A., & Ostwald, J. (1987). Different origins of cochlear efferents in some bat species, rats, and guinea pigs. Journal of Comparative Neurology 264(1), 56–72.Find this resource:

Azeredo, W. J., Kliment, M. L., Morley, B. J., Relkinn, E., Slepecky, N. B., Sterns, A., … Woods, C. I. (1999). Olivocochlear neurons in the chinchilla: A retrograde fluorescent labelling study. Hearing Research 134(1–2), 57–70Find this resource:

Bacon, S. P., & Viemeister, N. F. (1985). Temporal modulation transfer functions in normal-hearing and hearing-impaired listeners. Audiology: Official Organ of the International Society of Audiology 24(2), 117–134.Find this resource:

Bamiou, D. E., Musiek, F. E., & Luxon, L. M. (2001). Aetiology and clinical presentations of auditory processing disorders—a review. Archives of Disease in Childhood 85(5), 361–365.Find this resource:

Banks, M. I., & Smith, P. H. (1992). Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. Journal of Neuroscience 12(7), 2819–2837.Find this resource:

Bannan, N. (2012). Harmony and its role in human evolution. In N. Bannan (Ed.), Music, Language, and Human Evolution (pp. 288–339). Oxford, England: Oxford University Press.Find this resource:

Barsz, K., Benson, P. K., & Walton, J. P. (1998). Gap encoding by inferior collicular neurons is altered by minimal changes in signal envelope. Hearing Research 115(1–2), 13–26.Find this resource:

Baumann, S., Griffiths, T. D., Sun, L., Petkov, C. I., Thiele, A., & Rees, A. (2011). Orthogonal representation of sound dimensions in the primate midbrain. Nature Neuroscience 14(4), 423–425.Find this resource:

Bazwinsky, I., Bidmon, H. J., Zilles, K., & Hilbig, H. (2005). Characterization of the rhesus monkey superior olivary complex by calcium binding proteins and synaptophysin. Journal of Anatomy 207(6), 745–761.Find this resource:

Bazwinsky, I., Hilbig, H., Bidmon, H. J., & Rübsamen, R. (2003). Characterization of the human superior olivary complex by calcium binding proteins and neurofilament H (SMI-32). Journal of Comparative Neurology 456(3), 292–303.Find this resource:

Behrend, O., Brand, A., Kapfer, C., & Grothe, B. (2002). Auditory response properties in the superior paraolivary nucleus of the gerbil. Journal of Neurophysiology 87(6), 2915–2928.Find this resource:

Bertoncini, J., Serniclaes, W., & Lorenzi, C. (2009). Discrimination of speech sounds based upon temporal envelope versus fine structure cues in 5- to 7-year-old children. Journal of Speech, Language, and Hearing Research 52(3), 682–695.Find this resource:

Bidelman, G. M., & Bhagat, S. P. (2017). Cochlear, brainstem, and psychophysical responses show spectrotemporal tradeoff in human auditory processing. Neuroreport 28(1), 17–22.Find this resource:

Bledsoe, S. C., Snead, C. R., Helfert, R. H., Prasad, V., Wenthold, R. J., & Altschuler, R. A. (1990). Immunocytochemical and lesion studies support the hypothesis that the projection from the medial nucleus of the trapezoid body to the lateral superior olive is glycinergic. Brain Research 517(1–2), 189–194.Find this resource:

Brown, M. C., & Levine, J. L. (2008). Dendrites of medial olivocochlear neurons in mouse. Neuroscience 154(1), 147–159.Find this resource:

Bryant, G.A. (2013). Animal signals and emotion in music: Coordinating affect across groups. Frontiers in Psychology 4, 990.Find this resource:

Budinger, E., Brosch, M., Scheich, H., & Mylius, J. (2013). The subcortical auditory structures in the Mongolian gerbil: II. Frequency-related topography of the connections with cortical field AI. Journal of Comparative Neurology 521(12), 2772–2797.Find this resource:

Budinger, E., Heil, P., & Scheich, H. (2000). Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures. European Journal of Neuroscience 12(7), 2452–2474.Find this resource:

Caicedo, A., & Herbert, H. (1993). Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. Journal of Comparative Neurology 328(3), 377–392.Find this resource:

Caicedo, A., Kungel, M., Pujol, R., & Friauf, E. (1998). Glutamate-induced Co2+ uptake in rat auditory brainstem neurons reveals developmental changes in Ca2+ permeability of glutamate receptors. European Journal of Neuroscience 10(3), 941–954.Find this resource:

Caminos, E., García-Pino, E., Martínez-Galán, J. R., & Juiz, J. M. (2007). The potassium channel KCNQ5/Kv7.5 is localized in synaptic endings of auditory brainstem nuclei of the rat. The Journal of Comparative Neurology 505(4), 363–378.Find this resource:

Chirila, F. V., Rowland, K. C., Thompson, J. M., & Spirou, G. A. (2007). Development of gerbil medial superior olive: Integration of temporally delayed excitation and inhibition at physiological temperature. Journal of Physiology 584(Pt 1), 167–190.Find this resource:

Coomes, D. L., & Schofield, B. R. (2004). Projections from the auditory cortex to the superior olivary complex in guinea pigs. European Journal of Neuroscience 19(8), 2188–2200.Find this resource:

Coomes Peterson, D., & Schofield, B. R. (2007). Projections from auditory cortex contact ascending pathways that originate in the superior olive and inferior colliculus. Hearing Research 232(1–2), 67–77.Find this resource:

de Cheveigné, A. (1998). Cancellation model of pitch perception. Journal of the Acoustical Society of America 103(3), 1261–1271.Find this resource:

Dehmel, S., Kopp-Scheinpflug, C., Dörrscheidt, G. J., & Rübsamen, R. (2002). Electrophysiological characterization of the superior paraolivary nucleus in the Mongolian gerbil. Hearing Research 172(1–2), 18–36.Find this resource:

Dickson, C. T., Magistretti, J., Shalinsky, M. H., Fransén, E., Hasselmo, M. E., & Alonso, A. (2000). Properties and role of I(h) in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons. Journal of Neurophysiology 83(5), 2562–2579.Find this resource:

Drullman, R., Festen, J. M., & Plomp, R. (1994). Effect of temporal envelope smearing on speech reception. Journal of the Acoustical Society of America 95(2), 1053–1064.Find this resource:

Egnor, S. R., & Seagraves, K. M. (2016). The contribution of ultrasonic vocalizations to mouse courtship. Current Opinion in Neurobiology 38, 1–5.Find this resource:

Ehret, G. (2005). Infant rodent ultrasounds—a gate to the understanding of sound communication. Behavior Genetics 35(1), 19–29.Find this resource:

Ehret, G., & Bernecker, C. (1986). Low-frequency sound communication by mouse pups (Mus musculus): Wriggling calls release maternal behaviour. Animal Behaviour 34(3), 821–830.Find this resource:

Ehret, G., & Riecke, S. (2002). Mice and humans perceive multiharmonic communication sounds in the same way. Proceedings of the National Academy of Sciences of the United States of America 99(1), 479–482.Find this resource:

Falk, D. (2004). Prelinguistic evolution in early hominins: Whence motherese? The Behavioral and Brain Sciences 27(4), 491–503.Find this resource:

Feliciano, M., Saldaña, E., & Mugnaini, E. (1995). Direct projection from the rat primary auditory neocortex to the nucleus sagulum, paralemniscal regions, superior olivary complex and cochlear nuclei. Auditory Neuroscience 1(1), 287–308.Find this resource:

Felix, R. A., Fridberger, A., Leijon, S., Berrebi, A. S., & Magnusson, A. K. (2011). Sound rhythms are encoded by postinhibitory rebound spiking in the superior paraolivary nucleus. Journal of Neuroscience 31(35), 12566–12578.Find this resource:

Felix, R. A., Gourévitch, B., Gómez-Álvarez, M., Leijon, S. C. M., Saldaña, E., & Magnusson, A. K. (2017). Octopus cells in the posteroventral cochlear nucleus provide the main excitatory input to the superior paraolivary nucleus. Frontiers in Neural Circuits 11, 37.Find this resource:

Felix, R. A., & Magnusson, A. K. (2016). Development of excitatory synaptic transmission to the superior paraolivary and lateral superior olivary nuclei optimizes differential decoding strategies. Neuroscience 334(1), 1–12.Find this resource:

Felix, R. A., Magnusson, A. K., & Berrebi, A. S. (2015). The superior paraolivary nucleus shapes temporal response properties of neurons in the inferior colliculus. Brain Structure & Function 220(5), 2639–2652.Find this resource:

Felix, R. A., Vonderschen, K., Berrebi, A. S., & Magnusson, A. K. (2013). Development of on-off spiking in superior paraolivary nucleus neurons of the mouse. Journal of Neurophysiology 109(11), 2691–2704.Find this resource:

Fisahn, A., Yamada, M., Duttaroy, A., Gan, J.-W., Deng, C.-X., McBain, C. J., & Wess, J. (2002). Muscarinic induction of hippocampal gamma oscillations requires coupling of the M1 receptor to two mixed cation currents. Neuron 33(4), 615–624.Find this resource:

Fitch, T. W. (2006). The biology and evolution of music: A comparative perspective. Cognition 100(1), 173–215.Find this resource:

Ford, M. C., Grothe, B., & Klug, A. (2009). Fenestration of the calyx of Held occurs sequentially along the tonotopic axis, is influenced by afferent activity, and facilitates glutamate clearance. Journal of Comparative Neurology 514(1), 92–106.Find this resource:

Friauf, E. (2000). Development of chondroitin sulfate proteoglycans in the central auditory system of rats correlates with acquisition of mature properties. Audiology & Neuro-Otology 5(5) 251–262.Find this resource:

Friauf, E., Aragón, C., Löhrke, S., Westenfelder, B., & Zafra, F. (1999). Developmental expression of the glycine transporter GLYT2 in the auditory system of rats suggests involvement in synapse maturation. The Journal of Comparative Neurology 412(1), 17–37.Find this resource:

Friauf, E., & Ostwald, J. (1988). Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase. Experimental Brain Research 73(2), 263–284.Find this resource:

Frisina, R. D. (2001). Subcortical neural coding mechanisms for auditory temporal processing. Hearing Research 158(1–2), 1–27.Find this resource:

Fujino, K., Koyano, K., & Ohmori, H. (1997). Lateral and medial olivocochlear neurons have distinct electrophysiological properties in the rat brain slice. Journal of Neurophysiology 77(5), 2788–2804.Find this resource:

Gaub, S., & Ehret, G. (2005). Grouping in auditory temporal perception and vocal production is mutually adapted: The case of wriggling calls of mice. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 191(12), 1131–1135.Find this resource:

Geissler, D. B., & Ehret, G. (2002). Time-critical integration of formants for perception of communication calls in mice. Proceedings of the National Academy of Sciences of the United States of America 99(13), 9021–9025.Find this resource:

Gervain, J., & Werker, J. F. (2013). Prosody cues word order in 7-month-old bilingual infants. Nature Communications 4, 1490.Find this resource:

Golding, N. L., Ferragamo, M. J., & Oertel, D. (1999). Role of intrinsic conductances underlying responses to transients in octopus cells of the cochlear nucleus. The Journal of Neuroscience 19(8), 2897–2905.Find this resource:

Gómez-Álvarez, M., & Saldaña, E. (2016). Different tonotopic regions of the lateral superior olive receive a similar combination of afferent inputs. Journal of Comparative Neurology 524(11), 2230–2250.Find this resource:

González-Hernández, T., Mantolán-Sarmiento, B., González-González, B., & Pérez-González, H. (1996). Sources of GABAergic input to the inferior colliculus of the rat. Journal of Comparative Neurology 372(2), 309–326.Find this resource:

Goswami, U. (2015). Sensory theories of developmental dyslexia: three challenges for research. Nature Reviews: Neuroscience 16(1), 43–54.Find this resource:

Grimsley, J. M. S., Monaghan, J. J. M., & Wenstrup, J. J. (2011). Development of social vocalizations in mice. PloS One 6(3), e17460.Find this resource:

Grimsley, J. M. S., Sheth, S., Vallabh, N., Grimsley, C. A., Bhattal, J., Latsko, M., & Wenstrup, J. J. (2016). Contextual modulation of vocal behavior in mouse: Newly identified 12 khz “mid-frequency” vocalization emitted during restraint. Frontiers in Behavioral Neuroscience 10, 38.Find this resource:

Grothe, B. (1994). Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat. Journal of Neurophysiology 71(2), 706–721.Find this resource:

Grothe, B. (2000). The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Progress in Neurobiology 61(6), 581–610.Find this resource:

Gutfreund, Y., & Knudsen, E. I. (2006). Adaptation in the auditory space map of the barn owl. Journal of Neurophysiology 96(2), 813–825.Find this resource:

Hassfurth, B., Magnusson, A. K., Grothe, B., & Koch, U. (2009). Sensory deprivation regulates the development of the hyperpolarization-activated current in auditory brainstem neurons. European Journal of Neuroscience 30(7), 1227–1238.Find this resource:

Heffner, R.S. (2004). Primate hearing from a mammalian perspective. Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology 281(1), 1111–1122.Find this resource:

Hoffpauir, B. K., Marrs, G. S., Mathers, P. H., & Spirou, G. A. (2009). Does the brain connect before the periphery can direct? A comparison of three sensory systems in mice. Brain Research 1277, 115–129.Find this resource:

Holstege, G. (1998). The emotional motor system in relation to the supraspinal control of micturition and mating behavior. Behavioural Brain Research 92(2), 103–109.Find this resource:

Holstege, G., & Subramanian, H. H. (2016). Two different motor systems are needed to generate human speech. The Journal of Comparative Neurology 524(8), 1558–1577.Find this resource:

Holy, T. E., & Guo, Z. (2005). Ultrasonic songs of male mice. PloS Biology 3(12), e386.Find this resource:

Jain, R., & Shore, S. (2006). External inferior colliculus integrates trigeminal and acoustic information: Unit responses to trigeminal nucleus and acoustic stimulation in the guinea pig. Neuroscience Letters 395(1), 71–75Find this resource:

Jalabi, W., Kopp-Scheinpflug, C., Allen, P. D., Schiavon, E., DiGiacomo, R. R., Forsythe, I. D., & Maricich, S. M. (2013). Sound localization ability and glycinergic innervation of the superior olivary complex persist after genetic deletion of the medial nucleus of the trapezoid body. Journal of Neuroscience 33(38), 15044–15049.Find this resource:

Joris, P. X., Schreiner, C. E., & Rees, A. (2004). Neural processing of amplitude-modulated sounds. Physiological Reviews 84(2), 541–577.Find this resource:

Kadner, A., & Berrebi, A.S. (2008). Encoding of temporal features of auditory stimuli in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat. Neuroscience, 151(3) 868–887Find this resource:

Kadner, A., Kulesza, R. J., & Berrebi, A. S. (2006). Neurons in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat may play a role in sound duration coding. Journal of Neurophysiology 95(3), 1499–1508.Find this resource:

Kaiser, A., Alexandrova, O., & Grothe, B. (2011). Urocortin-expressing olivocochlear neurons exhibit tonotopic and developmental changes in the auditory brainstem and in the innervation of the cochlea. The Journal of Comparative Neurology 519(14), 2758–2778.Find this resource:

Kandler, K., Clause, A., & Noh, J. (2009). Tonotopic reorganization of developing auditory brainstem circuits. Nature Neuroscience 12(6), 711–717.Find this resource:

Kandler, K., & Friauf, E. (1995). Development of electrical membrane properties and discharge characteristics of superior olivary complex neurons in fetal and postnatal rats. European Journal of Neuroscience 7(8), 1773–1790.Find this resource:

Kelley, P. E., Frisina, R. D., Zettel, M. L., & Walton, J. P. (1992). Differential calbindin-like immunoreactivity in the brain stem auditory system of the chinchilla. Journal of Comparative Neurology 320(2), 196–212.Find this resource:

Klug, A., & Trussell, L. O. (2006). Activation and deactivation of voltage-dependent K+ channels during synaptically driven action potentials in the MNTB. Journal of Neurophysiology 96(3), 1547–1555.Find this resource:

Knudsen, E. I., & Konishi, M. (1978). A neural map of auditory space in the owl. Science 200(4343), 795–797.Find this resource:

Koch, U., & Grothe, B. (2003). Hyperpolarization-activated current (Ih) in the inferior colliculus: Distribution and contribution to temporal processing. Journal of Neurophysiology 90(6), 3679–3687.Find this resource:

Kopp-Scheinpflug, C., Pigott, B. M., & Forsythe, I. D. (2015). Nitric oxide selectively suppresses IH currents mediated by HCN1-containing channels. Journal of Physiology 593(7), 1685–1700.Find this resource:

Kopp-Scheinpflug, C., Tozer, A. J. B., Robinson, S. W., Tempel, B. L., Hennig, M. H., & Forsythe, I. D. (2011). The sound of silence: Ionic mechanisms encoding sound termination. Neuron 71(5), 911–925.Find this resource:

Krishna, B. S., & Semple, M. N. (2000). Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. Journal of Neurophysiology 84(1), 255–273.Find this resource:

Kuhl, P. K. (1986). Theoretical contributions of tests on animals to the special-mechanisms debate in speech. Experimental Biology 45(3), 233–265.Find this resource:

Kulesza, R. J. (2008). Cytoarchitecture of the human superior olivary complex: Nuclei of the trapezoid body and posterior tier. Hearing Research 241(1–2), 52–63.Find this resource:

Kulesza, R. J. (2014). Characterization of human auditory brainstem circuits by calcium-binding protein immunohistochemistry. Neuroscience 258, 318–331.Find this resource:

Kulesza, R. J., & Berrebi, A. S. (2000). Superior paraolivary nucleus of the rat is a GABAergic nucleus. Journal of the Association for Research in Otolaryngology 1(4), 255–269.Find this resource:

Kulesza, R. J., & Grothe, B. (2015). Yes, there is a medial nucleus of the trapezoid body in humans. Frontiers in Neuroanatomy 9, 35.Find this resource:

Kulesza, R. J., Kadner, A., & Berrebi, A. S. (2007). Distinct roles for glycine and GABA in shaping the response properties of neurons in the superior paraolivary nucleus of the rat. Journal of Neurophysiology 97(2), 1610–1620.Find this resource:

Kulesza, R. J., & Mangunay, K. (2008). Morphological features of the medial superior olive in autism. Brain Research 1200, 132–137.Find this resource:

Kulesza, R. J., Spirou, G. A., & Berrebi, A. S. (2003). Physiological response properties of neurons in the superior paraolivary nucleus of the rat. Journal of Neurophysiology 89(4), 2299–2312.Find this resource:

Kulesza, R. J., Viñuela, A., Saldaña, E., & Berrebi, A. S. (2002). Unbiased stereological estimates of neuron number in subcortical auditory nuclei of the rat. Hearing Research 168(1–2), 12–24.Find this resource:

Kuwabara, N., DiCaprio, R. A., & Zook, J. M. (1991). Afferents to the medial nucleus of the trapezoid body and their collateral projections. The Journal of Comparative Neurology 314(4), 684–706.Find this resource:

Kuwabara, N., & Zook, J. M. (1991). Classification of the principal cells of the medial nucleus of the trapezoid body. Journal of Comparative Neurology 314(4), 707–720.Find this resource:

Kuwabara, N., & Zook, J. M. (1992). Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats. Journal of Comparative Neurology 324(4), 522–538.Find this resource:

Kuwada, S., & Batra, R. (1999). Coding of sound envelopes by inhibitory rebound in neurons of the superior olivary complex in the unanesthetized rabbit. Journal of Neuroscience 19(6), 2273–2287.Find this resource:

Lange, S., Burda, H., Wegner, R. E., Dammann, P., Begall, S., & Kawalika, M. (2007). Living in a “stethoscope”: Burrow-acoustics promote auditory specializations in subterranean rodents. Die Naturwissenschafte 94(2), 134–138.Find this resource:

Langner, G. (1992). Periodicity coding in the auditory system. Hearing Research 60(2), 115–142.Find this resource:

LeDoux, J. E., Ruggiero, D. A., & Reis, D. J. (1985). Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. Journal of Comparative Neurology 242(2), 182–213.Find this resource:

Leijon, S., & Magnusson, A. K. (2014). Physiological characterization of vestibular efferent brainstem neurons using a transgenic mouse model. PloS One 9(5), e98277.Find this resource:

Leijon, S. C. M., Peyda, S., & Magnusson, A. K. (2016). Temporal processing capacity in auditory-deprived superior paraolivary neurons is rescued by sequential plasticity during early development. Neuroscience 337, 315–330.Find this resource:

Licklider, J. C. R. (1951). A duplex theory of pitch perception. Experientia 7(4), 128–133.Find this resource:

Lieberman, P. (2002). On the nature and evolution of the neural bases of human language. American Journal of Physical Anthropology 35, 36–62.Find this resource:

Liu, R. C., Linden, J. F., & Schreiner, C. E. (2006). Improved cortical entrainment to infant communication calls in mothers compared with virgin mice. European Journal of Neuroscience 23(11), 3087–3097.Find this resource:

Löhrke, S., Srinivasan, G., Oberhofer, M., Doncheva, E., & Friauf, E. (2005). Shift from depolarizing to hyperpolarizing glycine action occurs at different perinatal ages in superior olivary complex nuclei. The European Journal of Neuroscience 22(11), 2708–2722.Find this resource:

Lukose, R., Schmidt, E., Wolski, T. P., Murawski, N. J., & Kulesza, R. J. (2011). Malformation of the superior olivary complex in an animal model of autism. Brain Research 1398, 102–112.Find this resource:

Magnusson, A. K., Kapfer, C., Grothe, B., & Koch, U. (2005). Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset. Journal of Physiology 568(Pt 2), 497–512.Find this resource:

Malmierca, M. S., Cristaudo, S., Pérez-González, D., & Covey, E. (2009). Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. Journal of neuroscience 29(17), 5483–5493.Find this resource:

Mampe, B., Friederici, A. D., Christophe, A., & Wermke, K. (2009). Newborns’ cry melody is shaped by their native language. Current Biology 19(23), 1994–1997.Find this resource:

Marshall, A. F., Pearson, J. M., Falk, S. E., Skaggs, J. D., Crocker, W. D., Saldaña, E., & Fitzpatrick, D. C. (2008). Auditory response properties of neurons in the tectal longitudinal column of the rat. Hearing Research 244(1–2), 35–44.Find this resource:

McAlpine, D. (2005). Creating a sense of auditory space. Journal of Physiology 566, 21–28.Find this resource:

McCormick, D. A., & Huguenard, J. R. (1992). A model of the electrophysiological properties of thalamocortical relay neurons. Journal of Neurophysiology 566(Pt 1), 21–28.Find this resource:

Mikaelian, D. & Ruben, R.J. (1965) Development of Hearing in the Normal Cba-J Mouse: Correlation of Physiological Observations with Behavioral Responses and with Cochlear Anatomy. Acta oto-laryngologica, 59(2–6), 451–461.Find this resource:

Moore, J. K. (1987). The human auditory brain stem as a generator of auditory evoked potentials. Hearing Research 29(1), 33–43Find this resource:

Moore, J. K. (2000). Organization of the human superior olivary complex. Microscopy Research and Technique 51(4), 403–412.Find this resource:

Moore, J. K., Guan, Y. L., & Shi, S. R. (1998). MAP2 expression in developing dendrites of human brainstem auditory neurons. Journal of Chemical Neuroanatomy 16(1), 1–15.Find this resource:

Moore, J. K., & Moore, R. Y. (1971). A comparative study of the superior olivary complex in the primate brain. Folia Primatologica: International Journal of Primatology 16(1), 35–51.Find this resource:

Moore, J. K., Simmons, D. D., & Guan, Y. (1999). The human olivocochlear system: Organization and development. Audiology & Neuro-Otology 4(6), 311–325.Find this resource:

Motts, S. D., Slusarczyk, A. S., Sowick, C. S., & Schofield, B. R. (2008). Distribution of cholinergic cells in guinea pig brainstem. Neuroscience 154(1), 186–195.Find this resource:

Mulders, W.H., & Robertson, D. (2000). Evidence for direct cortical innervation of medial olivocochlear neurones in rats. Hearing Research 144(1–2), 65–72.Find this resource:

Musacchia, G., Sams, M., Skoe, E., & Kraus, N. (2007). Musicians have enhanced subcortical auditory and audiovisual processing of speech and music. Proceedings of the National Academy of Sciences of the United States of America 104(40), 15894–15898.Find this resource:

Nagtegaal, A. P., & Borst, J. G. G. (2010). In vivo dynamic clamp study of I(h) in the mouse inferior colliculus. Journal of Neurophysiology 104(2), 940–948.Find this resource:

Nelson, P. C., & Carney, L. H. (2004). A phenomenological model of peripheral and central neural responses to amplitude-modulated tones. The Journal of the Acoustical Society of America 116(4 Pt 1), 2173–2186.Find this resource:

Nelson, P. C., Smith, Z. M., & Young, E. D. (2009). Wide-dynamic-range forward suppression in marmoset inferior colliculus neurons is generated centrally and accounts for perceptual masking. Journal of Neuroscience 29(8), 2553–2562.Find this resource:

Oertel, D., Bal, R., Gardner, S. M., Smith, P. H., & Joris, P. X. (2000). Detection of synchrony in the activity of auditory nerve fibers by octopus cells of the mammalian cochlear nucleus. Proceedings of the National Academy of Sciences of the United States of America 97(22), 11773–11779.Find this resource:

Oliver, D. L., & Morest, D. K. (1984). The central nucleus of the inferior colliculus of the cat. Journal of Comparative Neurology 222, 237–264.Find this resource:

Ollo, C., & Schwartz, I. R. (1979). The superior olivary complex in C57BL/6 mice. American Journal of Anatomy 155(3), 349–373.Find this resource:

Panksepp, J. (2007). Neuroevolutionary sources of laughter and social joy: Modeling primal human laughter in laboratory rats. Behavioural Brain Research 182(2), 231–244.Find this resource:

Panksepp, J. (2015). Primal emotions and cultural evolution of language: Primal affects empower words. In U. M. Lüdtke (Ed.), Emotion in Language: Theory—research—application (pp. 27–48). Amsterdam, Netherlands: John Benjamins Publishing.Find this resource:

Panksepp, J., & Burgdorf, J. (2003). “Laughing” rats and the evolutionary antecedents of human joy? Physiology and Behavior 79(3), 533–547.Find this resource:

Panksepp, J., & Trevarthen, C. (2009). The neuroscience of emotion in music. In S. Malloch & C. Trevarthen (Eds.), Communicative musicality: Exploring the basis of human companionship (pp. 105–146). New York, NY: Oxford University Press.Find this resource:

Pape, H. C., & McCormick, D. A. (1989). Noradrenaline and serotonin selectively modulate thalamic burst firing by enhancing a hyperpolarization-activated cation current. Nature 340(6236), 715–718.Find this resource:

Park, Y.G., Park, H.Y., Lee, C. J., Choi, S., Jo, S., Choi, H., … Kim, D. (2010). Ca(V)3.1 is a tremor rhythm pacemaker in the inferior olive. Proceedings of the National Academy of Sciences of the United States of America, 107(23), 10731–10736.Find this resource:

Pérez-Reyes, E. (2003). Molecular physiology of low-voltage-activated t-type calcium channels. Physiological Reviews 83(1), 117–161.Find this resource:

Pihan, H., Tabert, M., Assuras, S., & Borod, J. (2008). Unattended emotional intonations modulate linguistic prosody processing. Brain and Language 105(2), 141–147.Find this resource:

Platzer, J., Engel, J., Schrott-Fischer, A., Stephan, K., Bova, S., Chen, H., Zheng, H, & Striessnig, J. (2000). Congenital deafness and sinoatrial node dysfunction in mice lacking class D L-type Ca2+ channels. Cell 102(1), 89–97.Find this resource:

Portfors, C. V. (2007). Types and functions of ultrasonic vocalizations in laboratory rats and mice. Journal of the American Association for Laboratory Animal Science 46(1), 28–34.Find this resource:

Rauschecker, J. P., & Shannon, R. V. (2002). Sending sound to the brain. Science 295(5557), 1025–1029.Find this resource:

Rees, A., & Palmer, A.R. (1989). Neuronal responses to amplitude-modulated and pure-tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise. Journal of the Acoustical Society of America 85(5), 1978–1994.Find this resource:

Rhode, W. S. (1998). Neural encoding of single-formant stimuli in the ventral cochlear nucleus of the chinchilla. Hearing Research 117(1–2), 39–56.Find this resource:

Roberts, M. T., Seeman, S. C., & Golding, N. L. (2014). The relative contributions of MNTB and LNTB neurons to inhibition in the medial superior olive assessed through single and paired recordings. Frontiers in Neural Circuits 8, 49.Find this resource:

Robinson, R. B., & Siegelbaum, S. A. (2003). Hyperpolarization-activated cation currents: From molecules to physiological function. Annual Review of Physiology 65, 453–480.Find this resource:

Rosen, S. (1992). Temporal information in speech: Acoustic, auditory and linguistic aspects. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 336(1278) 367–373.Find this resource:

Saldaña, E., Aparicio, M. A., Fuentes-Santamaría, V., & Berrebi, A. S. (2009). Connections of the superior paraolivary nucleus of the rat: Projections to the inferior colliculus. Neuroscience 163(1), 372–387.Find this resource:

Saldaña, E., Viñuela, A., Marshall, A. F., Fitzpatrick, D. C., & Aparicio, M. A. (2007). The TLC: A novel auditory nucleus of the mammalian brain. Journal of Neuroscience 27(48), 13108–13116.Find this resource:

Salimi, N., Zilany, M. S. A., & Carney, L. H. (2017). Modeling responses in the superior paraolivary nucleus: Implications for forward masking in the inferior colliculus. Journal of the Association for Research in Otolaryngology 18(3), 441–456Find this resource:

Sambeth, A., Ruohio, K., Alku, P., Fellman, V., & Huotilainen, M. (2008). Sleeping newborns extract prosody from continuous speech. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology 119(2), 332–341.Find this resource:

Sanes, D. H. (1993). The development of synaptic function and integration in the central auditory system. Journal of Neuroscience 13(6), 2627–2637.Find this resource:

Sanes, D. H., & Friauf, E. (2000). Review: Development and influence of inhibition in the lateral superior olivary nucleus. Hearing Research 147(1–2), 46–58.Find this resource:

Schmidt, E., Wolski, T. P., & Kulesza, R. J. (2010). Distribution of perineuronal nets in the human superior olivary complex. Hearing Research 265(1–2), 15–24.Find this resource:

Schofield, B. R. (1991). Superior paraolivary nucleus in the pigmented guinea pig: Separate classes of neurons project to the inferior colliculus and the cochlear nucleus. Journal of Comparative Neurology 312(1), 68–76.Find this resource:

Schofield, B. R. (1995). Projections from the cochlear nucleus to the superior paraolivary nucleus in guinea pigs. Journal of Comparative Neurology 360(1), 135–149.Find this resource:

Schofield, B. R., & Cant, N. B. (1991). Organization of the superior olivary complex in the guinea pig. I. Cytoarchitecture, cytochrome oxidase histochemistry, and dendritic morphology. Journal of Comparative Neurology 314(4), 645–670.Find this resource:

Schofield, B. R., & Cant, N. B. (1992). Organization of the superior olivary complex in the guinea pig: II. Patterns of projection from the periolivary nuclei to the inferior colliculus. Journal of Comparative Neurology 317(4), 438–455.Find this resource:

Schreiner, C. E., & Langner, G. (1988). Periodicity coding in the inferior colliculus of the cat. II. Topographical organization. Journal of Neurophysiology 60(6), 1823–1840.Find this resource:

Scott, L. L., Mathews, P. J., & Golding, N. L. (2005). Posthearing developmental refinement of temporal processing in principal neurons of the medial superior olive. Journal of Neuroscience 25(35), 7887–7895.Find this resource:

Shamma, S. A., & Micheyl, C. (2010). Behind the scenes of auditory perception. Current Opinion in Neurobiology 20(3), 361–366.Find this resource:

Shannon, R. V., Zeng, F. G., Kamath, V., Wygonski, J., & Ekelid, M. (1995). Speech recognition with primarily temporal cues. Science 270(5234), 303–304.Find this resource:

Simmons, D.D. (2002). Development of the inner ear efferent system across vertebrate species. Journal of Neurobiology 53(2), 228–250.Find this resource:

Simmons, D. D., Bertolotto, C., Typpo, K., Clay, A., & Wu, M. (1999). Differential development of cholinergic-like neurons in the superior olive: a light microscopic study. Anatomy and Embryology 200(6), 585–595.Find this resource:

Smith, P. H., Joris, P. X., Carney, L. H., & Yin, T. C. (1991). Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. Journal of Comparative Neurology 304(3), 387–407.Find this resource:

Smith, Z. M., Delgutte, B., & Oxenham, A. J. (2002). Chimaeric sounds reveal dichotomies in auditory perception. Nature 416(6876), 87–90.Find this resource:

Sommer, I., Lingenhöhl, K., & Friauf, E. (1993). Principal cells of the rat medial nucleus of the trapezoid body: an intracellular in vivo study of their physiology and morphology. Experimental Brain Research 95(2), 223–239.Find this resource:

Spangler, K. M., Warr, W. B., & Henkel, C. K. (1985). The projections of principal cells of the medial nucleus of the trapezoid body in the cat. The Journal of Comparative Neurology 238(3), 249–262.Find this resource:

Sparks, D. L., & Hartwich-Young, R. (1989). The deep layers of the superior colliculus. Reviews of Oculomotor Research 3, 213–255.Find this resource:

Spirou, G. A., Brownell, W. E., & Zidanic, M. (1990). Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. Journal of Neurophysiology 63(5), 1169–1190.Find this resource:

Stange, A., Myoga, M. H., Lingner, A., Ford, M. C., Alexandrova, O., Felmy, F., & Grothe, B. (2013). Adaptation in sound localization: from GABA (B) receptor-mediated synaptic modulation to perception. Nature Neuroscience 16(12), 1840–1847.Find this resource:

Sterenborg, J. C., Pilati, N., Sheridan, C. J., Uchitel, O. D., Forsythe, I. D., & Barnes-Davies, M. (2010). Lateral olivocochlear (LOC) neurons of the mouse LSO receive excitatory and inhibitory synaptic inputs with slower kinetics than LSO principal neurons. Hearing Research 270(1–2), 119–126.Find this resource:

Steriade, M., McCormick, D. A., & Sejnowski, T. J. (1993). Thalamocortical oscillations in the sleeping and aroused brain. Science 262(5134), 679–685.Find this resource:

Ströhmann, B., Schwarz, D. W., & Puil, E. (1994). Subthreshold frequency selectivity in avian auditory thalamus. Journal of Neurophysiology 71(4), 1361–1372.Find this resource:

Strominger, N. L., Nelson, L. R., & Dougherty, W. J. (1977). Second order auditory pathways in the chimpanzee. Journal of Comparative Neurology 172(2), 349–365.Find this resource:

Sun, H., & Wu, S. H. (2008). Modification of membrane excitability of neurons in the rat’s dorsal cortex of the inferior colliculus by preceding hyperpolarization. Neuroscience 154(1), 257–272.Find this resource:

Tan, M. L., Theeuwes, H. P., Feenstra, L., & Borst, J. G. G. (2007). Membrane properties and firing patterns of inferior colliculus neurons: An in vivo patch-clamp study in rodents. Journal of Neurophysiology 98(1), 443–453.Find this resource:

Thompson, A. M., & Thompson, G. C. (1991). Posteroventral cochlear nucleus projections to olivocochlear neurons. Journal of Comparative Neurology 303(2), 267–285.Find this resource:

Thompson, G. C., & Thompson, A. M. (1986). Olivocochlear neurons in the squirrel monkey brainstem. Journal of Comparative Neurology 254(2), 246–258.Find this resource:

Tollin, D. J. (2003). The lateral superior olive: A functional role in sound source localization. The Neuroscientist: A Review Journal Bringing Neurobiology, Neurology and Psychiatry 9(2), 127–143.Find this resource:

Tóth, I. E., Boldogkoi, Z., Medveczky, I., & Palkovits, M. (1999). Lacrimal preganglionic neurons form a subdivision of the superior salivatory nucleus of rat: Transneuronal labelling by pseudorabies virus. Journal of the Autonomic Nervous System 77(1), 45–54.Find this resource:

Trevarthen, C., & Delafield-Butt, J. T. (2013). Autism as a developmental disorder in intentional movement and affective engagement. Frontiers in Integrative Neuroscience 7, 49.Find this resource:

Vetter, D. E., Saldaña, E., & Mugnaini, E. (1993). Input from the inferior colliculus to medial olivocochlear neurons in the rat: a double label study with PHA-L and cholera toxin. Hearing Research 70(2), 173–186.Find this resource:

Viñuela, A., Aparicio, M. A., Berrebi, A. S., & Saldaña, E. (2011). Connections of the Superior Paraolivary Nucleus of the Rat: II. Reciprocal Connections with the Tectal Longitudinal Column. Frontiers in Neuroanatomy 5, 1.Find this resource:

Wang, J., Zhou, R., & Gao, W. (2017). The neural pathway for lacrimal gland tear secretion in New Zealand White rabbits. Neuroscience Letters 649, 14–19.Find this resource:

Warr, W. B. (1966). Fiber degeneration following lesions in the anterior ventral cochlear nucleus of the cat. Experimental Neurology 14(4), 453–474.Find this resource:

Warr, W. B. (1975). Olivocochlear and vestibular efferent neurons of the feline brain stem: Their location, morphology and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. Journal of Comparative Neurology 161(2), 159–181.Find this resource:

Warr, W. B., Beck Boche, J. E., Ye, Y., & Kim, D. O. (2002). Organization of olivocochlear neurons in the cat studied with the retrograde tracer cholera toxin-B. Journal of the Association for Research in Otolaryngology 3(4), 457–478.Find this resource:

White, J. S., & Warr, W. B. (1983). The dual origins of the olivocochlear bundle in the albino rat. Journal of Comparative Neurology 219(2), 203–214.Find this resource:

Wilson, B. S., Finley, C. C., Lawson, D. T., Wolford, R. D., Eddington, D. K., & Rabinowitz, W. M. (1991). Better speech recognition with cochlear implants. Nature 352(6332), 236–238.Find this resource:

Winter, I. M., Robertson, D., & Cole, K. S. (1989). Descending projections from auditory brainstem nuclei to the cochlea and cochlear nucleus of the guinea pig. Journal of Comparative Neurology 280(1), 143–157.Find this resource:

Yang, L. C., & Pollak, G. D. (1997). Differential response properties to amplitude modulated signals in the dorsal nucleus of the lateral lemniscus of the mustache batand the roles of GABAergic inhibition. Journal of Neurophysiology 77(1), 324–340.Find this resource:

Yao, W., & Godfrey, D. A. (1998). Immunohistochemical evaluation of cholinergic neurons in the rat superior olivary complex. Microscopy Research and Technique 41(3), 270–283.Find this resource:

Yassin, L., Radtke-Schuller, S., Asraf, H., Grothe, B., Hershfinkel, M., Forsythe, I. D., & Kopp-Scheinpflug, C. (2014). Nitric oxide signaling modulates synaptic inhibition in the superior paraolivary nucleus (SPN) via cGMP-dependent suppression of KCC2. Frontiers in Neural Circuits 8, 65.Find this resource:

Yasui, Y., Nakano, K., & Mizuno, N. (1992). Descending projections from the subparafascicular thalamic nucleus to the lower brain stem in the rat. Experimental Brain Research 90(3), 508–518.Find this resource:

Zheng, Y., & Escabí, M. A. (2008). Distinct roles for onset and sustained activity in the neuronal code for temporal periodicity and acoustic envelope shape. Journal of Neuroscience 28(52), 14230–14244.Find this resource:

Zook, J. M., & Casseday, J. H. (1985). Projections from the cochlear nuclei in the mustache bat, Pteronotus parnellii. Journal of Comparative Neurology 237(3), 307–324.Find this resource: