Connections of the superior paraolivary nucleus of the rat: projections to the inferior colliculus

Abstract

GABAergic neurotransmission contributes to shaping the response properties of inferior colliculus (IC) neurons. In rodents, the superior paraolivary nucleus (SPON) is a prominent and well-defined cell group of the superior olivary complex that sends significant but often neglected GABAergic projections to the IC. To investigate the trajectory, distribution and morphology of these projections, we injected the neuroanatomical tracer biotinylated dextran amine into the SPON of albino rats. Our results demonstrate that: 1) The SPON innervates densely all three subdivisions of the ipsilateral IC: central nucleus (CNIC), dorsal cortex (DCIC) and external cortex (ECIC). The SPON also sends a sparse projection to the contralateral DCIC via the commissure of the IC. 2) SPON axons are relatively thick (diameter > 1.2 μm), ascend to the midbrain tectum in the medial aspect of the lateral lemniscus, and, for the most part, do not innervate the nuclei of the lateral lemniscus. 3) SPON fibers ramify profusely within the IC and bear abundant en passant and terminal boutons. 4) The axons of neurons in discrete regions of the SPON form two laminar terminal plexuses in the ipsilateral IC: a medial plexus that spans the CNIC and DCIC parallel to the known fibrodendritic laminae of the CNIC, and a lateral plexus located in the ECIC and oriented more or less parallel to the surface of the IC. 5) The projection from SPON to the ipsilateral IC is topographic: medial SPON neurons innervate the ventromedial region of the CNIC and DCIC and the ventrolateral region of the ECIC, whereas more laterally situated SPON neurons innervate more dorsolateral regions of the CNIC and DCIC and more dorsomedial regions of the ECIC. Thus, SPON fibers follow a pattern of distribution within the IC similar to that previously reported for intracollicular and corticocollicular projections.

Development of on-off spiking in superior paraolivary nucleus neurons of the mouse

“…There is evidence for an excitatory input to the SPON from the contralateral cochlear nucleus (Friauf and Ostwald 1988;Kuwabara et al 1991;Thompson and Thompson 1991;Schofield 1995;Saldaña et al 2009) and tentative evidence for a specific input from the specialized octopus neurons (Friauf and Ostwald 1988;Schofield 1995;Saldaña et al 2009). The responses of octopus neurons are triggered by the onsets of sounds (Godfrey et al 1975;Rhode and Smith 1986) and exhibit extremely precise spike timing.…”

“…It seems safe to assume that at least some aspects of the temporal sound code related to periodicity are inherited from the auditory brain stem (Palombi and Caspary 1996;Koch and Grothe 1998;Backoff et al 1999;Zhang and Kelly 2003;Caspary et al 2002). The SPON is a prime candidate for conveying such temporal information to the IC, as it provides one of the major ascending inputs (Kelly et al 1998;Saldaña and Berrebi 2000;Saldaña et al 2009). Inhibition in the IC also contributes to more complex processing of acoustic signals, such as computing the difference in temporal envelopes across frequency (Li et al 2006), forward masking of sound amplitude modulations (Nelson et al 2009), and discrimination of species-specific communication calls (Klug et al 2002), all of which are important mechanisms for behaviorally relevant sounds.…”

“…SPON neurons are also capable of signaling the presence of short gaps within ongoing sound stimuli (Kadner and Berrebi 2008). Thus, SPON neurons are well suited to faithfully transmit temporal information via their GABAergic projections to the inferior colliculus (IC), a major site of sensory integration located in the midbrain (Schofield 1991;Kulesza and Berrebi 2000;Saldaña and Berrebi 2000;Saldaña et al 2009). …”

The function of offset neurons in auditory information processing

“…In this way, offset responses encode the special sound information carried by sound signal. Some onset-offset cells are also found in the auditory midbrain [93,96], which may be attributed to the convergent projections from VNLL onset encoding and SPN offset responses to IC.…”

“…Koop-Scheinpflug et al [40] [68,89]. Given that cells within the ventral nucleus of the lateral lemniscus (VNLL) respond to tones with a single precise onset response [90,91], and that SPON and VNLL neurons are respectively GABAergic and glycinergic, and both provide inhibition to the ipsilateral IC [92,93], the convergent inputs from SPON and VNLL to IC may explain the onset-offset responses with IPSPs both at the onset and offset of the tone in the auditory midbrain [94][95][96]. These speculations might suggest that offset neurons (except onset-sustainedoffset type) that arise de novo in some auditory nuclei maintain their original function, while some inherit ascending synaptic information [31], which also suggest that onset and offset responses may be encoded by distinct acoustic channels.…”