Projections of the pontine nuclei to the cochlear nucleus in rats

Abstract

In the cochlear nucleus, there is a magnocellular core of neurons whose axons form the ascending auditory pathways. Surrounding this core is a thin shell of microneurons called the granule cell domain (GCD). The GCD receives auditory and nonauditory inputs and projects in turn to the dorsal cochlear nucleus, thus appearing to serve as a central locus for integrating polysensory information and descending feedback. Nevertheless, the source of many of these inputs and the nature of the synaptic connections are relatively unknown. We used the retrograde tracer Fast Blue to demonstrate that a major projection arises from the contralateral pontine nuclei (PN) to the GCD. The projecting cells are more densely located in the ventral and rostral parts of the PN. They also are clustered into a lateral and a medial group. Injections of anterograde tracers into the PN labeled mossy fibers in the contralateral GCD. The terminals are confined to those parts of the GCD immediately surrounding the ventral cochlear nucleus. There is no PN projection to the dorsal cochlear nucleus. These endings have the form of bouton and mossy fiber endings as revealed by light and electron microscopy. The PN represent a key station between the cerebral and cerebellar cortices, so the pontocochlear nucleus projection emerges as a significant source of highly processed information that is introduced into the early stages of the auditory pathway. The cerebropontocerebellar pathway may impart coordination and timing cues to the motor system. In an analogous way, perhaps the cerebropontocochlear nucleus projection endows the auditory system with a timing mechanism for extracting temporal information.

Primary innervation of the avian and mammalian cochlear nucleus

“…The unmyelinated type II auditory nerve fibers, which carry information from the outer hair cells of the cochlea, terminate among the granule cells [11,22], but the myelinated type I fibers do not [23,51]. The GCD does receive nonauditory inputs, including projections from the somatosensory cuneate nucleus [216,219], the trigeminal nuclei [74], the vestibular system [25,26,84], and pontine nuclei [131]. Many of the inputs are in the form of mossy fiber endings [65,122,131,219] and at least some are immunoreactive to the neurotransmitter, glutamate [219].…”

Synaptic influences of pontine nuclei on cochlear nucleus cells

“…In the IWB preparation, these latency values most likely correspond to disynaptic transmission (Babalian et al 1997(Babalian et al , 1999(Babalian et al , 2002. As both the AVCN cells extended their dendrites to the GCD and the PN input to GCD was shown to be excitatory (Ohlrogge et al 2001), the most probable mechanism of observed disynaptic EPSPs would be an excitation of the granule cells by PN projections and following excitatory action from granule cells to target cells. The large majority of other responses in the present study were IPSPs at longer latencies (5.3 ms and longer), suggesting the involvement of additional synaptic relays.…”

“…An additional or alternative mechanism for polysynaptic inhibition of pyramidal cells from PN may function through a cerebellum-like circuit of the DCN (reviewed in Oertel and Young 2004) and would include PN-GCD-carthweel cell-pyramidal cells synaptic pathway. Even if no PN endings were found in the layer 2 of the DCN containing granule cells (Ohlrogge et al 2001), such a pathway may function through granule cells in all other CN areas known to send parallel fibers to the DCN (Mugnaini et al 1980b). It should also be noted that additional synaptic relays in the GCD and/or within the magnocellular CN core, including, for example, Golgi cells, unipolar brush cells, interneurons, and CN cells projecting to the contralateral CN, may account for PNinduced responses with very long latencies.…”

“…However, it is possible that, for some reason (e.g., cell size, location in the CN), we did not penetrate CN cells projecting to PN. A tracing study in rats (Ohlrogge et al 2001) has demonstrated that projections from the contralateral PN to the CN outnumbered the ipsilateral projections by about four times. Our data are not in accordance with these observations, as comparable proportions of neurons were influenced by the stimulation of the ipsilateral and contralateral PN.…”

“…Thus, the GCD, which is considered as a shell of the CN (see for review Ryugo et al 2003), is well positioned to integrate a variety of non-auditory information and feedback auditory inputs to modulate the output activity of neurons in the CN core (VCN and DCN). A recent neuroanatomical study has demonstrated the existence of prominent bilateral projections from pontine nuclei (PN) to the CN, also terminating principally in the GCD of the CN (Ohlrogge et al 2001). The aim of the present work was to assess the physiological properties of PN inputs to the CN cells.…”