Regeneration, Repair, and Developmental NeuroscienceResearch PaperGlutamatergic inputs and glutamate-releasing immature inhibitory inputs activate a shared postsynaptic receptor population in lateral superior olive
Highlights
▶The mature lateral superior olive receives glutamatergic and glycinergic inputs. ▶The immature glycinergic inputs also release glutamate. ▶We asked whether these pathways could engage in glutamatergic crosstalk. ▶Glutamate spillover can activate NMDA receptors shared by both pathways. ▶Shared NMDA receptors may be proximal to classic glutamatergic synapses.
Section snippets
Slice preparation
Sprague–Dawley rats born to animals bred on site or shipped pregnant (Charles River Laboratories, Wilmington, MA, USA) were used; all procedures were performed in accord with Canadian Council on Animal Care guidelines and were previously approved by the Animal Review Ethics Board of McMaster University. Rat pups aged P3–P8 were deeply anesthetized (isoflurane), and the brain was quickly removed and placed in ice-cold artificial cerebrospinal fluid (ACSF) containing (in mM): NaCl, 124; MgSO4, 1;
Glutamate spillover at room temperature
As glutamate release at MNTB–LSO synapses is most prevalent before P9, we focused on slices from animals age P3–P8. Little is known about the subcellular position of synapses in the immature LSO, and we asked whether synapses under the two pathways were sufficiently close to be within each other's glutamate diffusion radius at room temperature. To test for the possibility of spillover, we located LSO principal cells that showed a mixed GABA/glycine/glutamate response to MNTB stimulation (Fig. 1
Discussion
In rodent auditory brainstem, expression of VGLUT3 allows glutamate release from immature inhibitory terminals during the first postnatal week, and before P9 a majority of LSO principal neurons exhibit a glutamatergic response to stimulation of the MNTB pathway (Gillespie et al., 2005), as well of course to stimulation of the AVCN pathway (Ene et al., 2003). Investigating the possibility of glutamate spillover in the LSO, we found that stimulation of either pathway resulted in the activation of
Acknowledgments
This study was supported by infrastructure funds from the Canadian Foundation for Innovation, an operating grant from the Canadian Institutes for Health Research (D.C.G.), and a CONACyT postdoctoral fellowship (J.A.). The authors would like to thank Dan Case and Dan Goldreich for comments on the manuscript.
References (52)
- et al.
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 Res
(1990) - et al.
Development of precise maps in visual cortex requires patterned spontaneous activity in the retina
Neuron
(2005) - et al.
Synaptic changes underlying the strengthening of GABA/glycinergic connections in the developing lateral superior olive
Neuroscience
(2010) - et al.
Ectopic release of synaptic vesicles
Neuron
(2003) - et al.
Development of the base of the cochlea: place code shift in the gerbil
Hear Res
(1998) - et al.
Developmental and regional expression in the rat brain and functional properties of four NMDA receptors
Neuron
(1994) - et al.
Obligatory role of NR2A for metaplasticity in visual cortex
Neuron
(2007) - et al.
Hippocampal synapses: do they talk to their neighbours?
Trends Neurosci
(1999) - et al.
Ion fluxes associated with excitatory amino acid transport
Neuron
(1995) - et al.
Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus
J Neurosci
(1998)
Ventral cochlear nucleus responses to contralateral sound are mediated by commissural and olivocochlear pathways
J Neurophysiol
Binaural interaction in the cat superior olive S segment
J Neurophysiol
A burst-based “Hebbian” learning rule at retinogeniculate synapses links retinal waves to activity-dependent refinement
PLoS Biol
Processing of binaural stimuli by cat superior olivary complex neurons
Exp Brain Res
Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei
J Comp Neurol
Prolonged synaptic currents and glutamate spillover at the parallel fiber to stellate cell synapse
J Neurosci
Pre- and post-synaptic properties of glutamatergic transmission in the immature inhibitory MNTB-LSO pathway
J Neurophysiol
Functional refinement in the projection from ventral cochlear nucleus to lateral superior olive precedes hearing onset in rat
PLoS One
Glutamatergic calcium responses in the developing lateral superior olive: receptor types and their specific activation by synaptic activity patterns
J Neurophysiol
Inhibitory synapses in the developing auditory system are glutamatergic
Nat Neurosci
Burst-induced anti-Hebbian depression acts through short-term synaptic dynamics to cancel redundant sensory signals
J Neurosci
Mechanisms underlying development of visual maps and receptive fields
Annu Rev Neurosci
Block of N-methyl-d-aspartate-activated current by the anticonvulsant MK-801: selective binding to open channels
Proc Natl Acad Sci U S A
Contralateral inhibitory and excitatory frequency response maps in the mammalian cochlear nucleus
Eur J Neurosci
Tonotopic reorganization of developing auditory brainstem circuits
Nat Neurosci
Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation
Nat Neurosci
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