Time Course and Permeation of Synaptic AMPA Receptors in Cochlear Nuclear Neurons Correlate with Input

Abstract

AMPA receptors mediate rapid glutamatergic synaptic transmission. In the mammalian cochlear nuclei, neurons receive excitatory input from either auditory nerve fibers, parallel fibers, or both fiber systems. The functional correlates of differences in the source of input were examined by recording AMPA receptor-mediated, miniature EPSCs (mEPSCs) in whole-cell voltage-clamp mode from identified neurons. Bushy, octopus, and T-stellate cells of the ventral cochlear nucleus (VCN) and tuberculoventral cells of the dorsal cochlear nucleus (DCN) receive most of their excitatory input from the auditory nerve; fusiform cells receive excitatory inputs from both the auditory nerve and parallel fibers; cartwheel cells receive excitatory input from parallel fibers alone. mEPSCs from bushy, octopus, T-stellate, and tuberculoventral cells had significantly faster decay time constants (0.35-0.40 msec) than did those from fusiform and cartwheel cells (1.32-1.79 msec). Some fusiform cells had two populations of mEPSCs with distinct time courses. mEPSCs in cells with auditory nerve input alone were inhibited by philanthotoxin, a blocker of calcium-permeable AMPA receptors, whereas mEPSCs in cells with parallel fiber input were not. Thus AMPA receptors postsynaptic to the auditory nerve differ from those postsynaptic to parallel fibers both in channel-gating kinetics and in their permeability to calcium. These results confirm the conclusion that synaptic AMPA receptors are specialized according to the source of input (Hunter et al., 1993; Rubio and Wenthold, 1997; Wang et al., 1998).

Fast Synaptic Currents inDrosophilaMushroom Body Kenyon Cells Are Mediated by α-Bungarotoxin-Sensitive Nicotinic Acetylcholine Receptors and Picrotoxin-Sensitive GABA Receptors

“…This suggests that the basic properties of receptors mediating fast excitatory synaptic transmission can be similar, even in distinct populations of neurons, distinguished by the neurotransmitter phenotype or anatomical grouping. This is not entirely unexpected, given that the kinetic properties of AMPA-receptor-mediated mEPSCs in the mammalian CNS can be similar in anatomically and functionally distinct neuronal subpopulations (Gardner et al, 1999;Simkus and Stricker, 2002). More detailed analysis of receptor properties in distinct cell types, identified using enhancer trap lines defining specific neuronal subtypes, may reveal differences in functional properties not detected in the present study.…”

A biophysical model for modulation frequency encoding in the cochlear nucleus

“…For T-stellate and vertical cells there are 10 AN fibers (4 HSR, 3 MSR and 3 LSR) coming from a single channel of the auditory periphery model (the central CF) and their inputs are always filtered by the dendrite. For D-stellate there are 10 AN fibers with the same type distribu- We modeled the synapses in the button endings using a doubleexponential alpha function, with parameters adjusted in order to reproduce the results obtained in Gardner et al (1999) for stellate and vertical post-synaptic currents.…”

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

“…There are several shared features of temporal coding circuits in birds and mammals. These include accurate phase locking in the auditory nerve, presynaptic specializations to make neurotransmitter release both precise and modifiable, postsynaptic specializations, including specific glutamate receptors, potassium conductances and characteristic neuronal morphology (for reviews see [30,79]). …”

“…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.…”