Correlation of AMPA Receptor Subunit Composition with Synaptic Input in the Mammalian Cochlear Nuclei

Abstract

The composition of AMPA receptors in patches excised from somata and dendrites of six cell types in the mammalian cochlear nuclei was probed and compared electrophysiologically and pharmacologically with the rapid application of glutamate. Cells excited predominantly by auditory nerve fibers had AMPA receptors with exceptionally rapid gating (submillisecond deactivation and desensitization time constants). The nonlinear current-voltage relationship in the presence of spermine showed that few of these receptors had GluR2 subunits, and the insensitivity of desensitization to cyclothiazide indicated that they contained mostly flop splice variants. At synapses made by parallel fibers, AMPA receptors were slowly gating (time constants of deactivation and desensitization >1 msec) and contained higher levels of GluR2 and flip isoforms. However, receptors at auditory nerve synapses on cells that also receive parallel fiber input, the fusiform cells, had intermediate properties with respect to kinetics and contained GluR2 and flip isoforms. Given the diverse biophysical properties, patterns of innervation, patterns of electrical activity, and targets of each cell type in vivo, these data indicate that the kinetics and permeation properties of AMPA receptors are linked to factors associated with synaptic connectivity.

Bidirectional synaptic plasticity in the cerebellum-like mammalian dorsal cochlear nucleus

“…In the present experiments that were performed under voltage-clamp, the contribution of voltage-gated Ca 2ϩ currents was presumably small; but under physiological conditions, voltage-gated Ca 2ϩ currents are prominent in cartwheel cells, where they underlie the complex action potential (23,24), and have been demonstrated in fusiform cells (25). AMPA receptors differ at the three groups of synapses in fusiform and cartwheel cells but all contain GluR2 and are thus not permeable to Ca 2ϩ (16,26,27). NMDA receptors are Ca 2ϩ -permeable and contribute to excitation of fusiform and cartwheel cells by parallel fibers (14,28,29).…”

Single Granule Cells Excite Golgi Cells and Evoke Feedback Inhibition in the Cochlear Nucleus

“…The difference in the IV relations between the spermine-containing and spermine-free recording conditions was significant at a holding potential of ϩ60 mV (p Ͻ 0.05, unpaired t test). These results indicate that EPSCs are mediated, at least partly, by Ca ϩ2 -permeable AMPARs (Gardner et al, 2001;Liu and Cull-Candy, 2002), as in the cerebellum (but see Menuz et al, 2008;Cesana et al, 2013). The results also support the hypothesis that Ca 2ϩ permeability of AMPARs is target dependent in cochlear nucleus because stellate cell target AMPARs are also Ca 2ϩ permeable (Apostolides and Trussell, 2014) whereas cartwheel and fusiform cell target AMPARs are not (Gardner et al, 1999(Gardner et al, , 2001.…”

Coding interaural time differences at low best frequencies in the barn owl

“…The brevity of these currents depends not only on the time course of release but also on the specific properties of the postsynaptic AMPA receptors. AMPA receptors in time coding auditory neurons have fast kinetics and rapid desensitization rates, leading to very short EPSCs [30][31][32]88]. Although brief EPSCs underlie the rapid synaptic potential changes seen in time coding neurons, the intrinsic electrical properties of these neurons also shape the synaptic response as well as the temporal firing pattern.…”