Expression of glutamate and inhibitory amino acid vesicular transporters in the rodent auditory brainstem

Abstract

Glutamate is the main excitatory neurotransmitter in the auditory system, but associations between glutamatergic neuronal populations and the distribution of their synaptic terminations have been difficult. Different subsets of glutamatergic terminals employ one of three vesicular glutamate transporters (VGLUT) to load synaptic vesicles. Recently, VGLUT1 and VGLUT2 terminals were found to have different patterns of organization in the inferior colliculus suggesting that there are different types of glutamatergic neurons in the brainstem auditory system with projections to the colliculus. To positively identify VGLUT-expressing neurons as well as inhibitory neurons in the auditory brainstem, we used in situ hybridization to identify the mRNA for VGLUT1, VGLUT2, and VIAAT (the vesicular inhibitory amino acid transporter used by GABAergic and glycinergic terminals). Similar expression patterns were found in subsets of glutamatergic and inhibitory neurons in the auditory brainstem and thalamus of adult rats and mice. Four patterns of gene expression were seen in individual neurons. 1) VGLUT2 expressed alone was the prevalent pattern. 2) VGLUT1 co-expressed with VGLUT2 was seen in scattered neurons in most nuclei but was common in the medial geniculate body and ventral cochlear nucleus. 3) VGLUT1 expressed alone was found only in granule cells. 4) VIAAT expression was common in most nuclei but dominated in some. These data show that the expression of the VGLUT1/2 and VIAAT genes can identify different subsets of auditory neurons. This may facilitate the identification of different components in auditory circuits.

Conductive Hearing Loss Has Long-Lasting Structural and Molecular Effects on Presynaptic and Postsynaptic Structures of Auditory Nerve Synapses in the Cochlear Nucleus

“…The physiological consequences of an increase of the GluA3 subunit for synaptic transmission in the cochlear nucleus need further investigations, but it could well be that the decay times of excitatory currents are slower in response to earplugging. This can happen, for example, if the ratio of GluA3 flip/flop isoforms is higher at the endbulb synapse in earplugged animals (Mosbacher et al, 1994;Gardner et al, 2001). This could provide a stronger excitatory input that will compensate for the reduction in sensory input.…”

“…Manipulation of in vivo sensory experience also produces homeostatic changes at cortical synapses. Depriving vision from 2 to up to 7 d scales up excitatory synapses in the visual cortex pyramidal neurons, by incorporating more GluA1 AMPAR subunits, whereas reexposing the visually deprived animals to light scales down the synapses (Goel et al, 2006(Goel et al, , 2011Goel and Lee, 2007). Interestingly, the sensory experience-induced homeostatic synaptic changes are mainly observed as regulation of the amplitude rather than the frequency of AMPA-mEPSCs.…”

“…More recently, it has become clear that other forms of hearing impairment associated with conductive hearing loss can also alter synaptic transmission in central auditory regions (Xu et al, 2007(Xu et al, , 2010. However, despite being the second most prevalent form of hearing loss, conductive hearing loss and its effects on central synapses have received relatively little attention.…”

“…1A;Ryugo and Fekete, 1982;Rouiller et al, 1986). Endbulb synapses contain AMPAR subunits with rapid kinetics (GluA3 and GluA4; Wang et al, 1998;Gardner et al, 1999Gardner et al, , 2001Whiting et al, 2009). The slower GluA1 subunit is absent at mature endbulb synapses, and the GluA2 subunit, whose absence is associated with fast synapses, is expressed at very low levels (Wang et al, 1998;Gardner et al, 1999Gardner et al, , 2001.…”

“…Endbulb synapses contain AMPAR subunits with rapid kinetics (GluA3 and GluA4; Wang et al, 1998;Gardner et al, 1999Gardner et al, , 2001Whiting et al, 2009). The slower GluA1 subunit is absent at mature endbulb synapses, and the GluA2 subunit, whose absence is associated with fast synapses, is expressed at very low levels (Wang et al, 1998;Gardner et al, 1999Gardner et al, , 2001. Bushy cells are a major cell type in the anteroventral cochlear nucleus, and they enhance the temporal fine structure information that is present in the phase-locked pattern of auditory nerve spikes (Joris et al, 1994).…”