A Role for Short-Term Synaptic Facilitation and Depression in the Processing of Intensity Information in the Auditory Brain Stem

Abstract

The nature of the synaptic connection from the auditory nerve onto the cochlear nucleus neurons has a profound impact on how sound information is transmitted. Short-term synaptic plasticity, by dynamically modulating synaptic strength, filters information contained in the firing patterns. In the sound-localization circuits of the brain stem, the synapses of the timing pathway are characterized by strong short-term depression. We investigated the short-term synaptic plasticity of the inputs to the bird's cochlear nucleus angularis (NA), which encodes intensity information, by using chick embryonic brain slices and trains of electrical stimulation. These excitatory inputs expressed a mixture of short-term facilitation and depression, unlike those in the timing nuclei that only depressed. Facilitation and depression at NA synapses were balanced such that postsynaptic response amplitude was often maintained throughout the train at high firing rates (>100 Hz). The steady-state input rate relationship of the balanced synapses linearly conveyed rate information and therefore transmits intensity information encoded as a rate code in the nerve. A quantitative model of synaptic transmission could account for the plasticity by including facilitation of release (with a time constant of approximately 40 ms), and a two-step recovery from depression (with one slow time constant of approximately 8 s, and one fast time constant of approximately 20 ms). A simulation using the model fit to NA synapses and auditory nerve spike trains from recordings in vivo confirmed that these synapses can convey intensity information contained in natural train inputs.

Morphological and Functional Continuum Underlying Heterogeneity in the Spiking Fidelity at the Calyx of Held SynapseIn Vitro

“…Synapses with high P r , small RRPs, and strong STD appear well-suited for coding ITDs (Kuba et al, 2002;Cook et al, 2003;Yang and Xu-Friedman, 2009;Couchman et al, 2010), whereas synapses with low P r , large RRPs, and STF followed by slow depression are better tuned for coding ILDs (MacLeod et al, 2007;Yang and Xu-Friedman, 2009). Thus, it is tempting to speculate that calyces with simple morphologies filter timing information, those with complex morphologies filter intensity information, and those with intermediate morphologies filter a combination of both.…”

The Role of Presynaptic Dynamics in Processing of Natural Spike Trains in Hippocampal Synapses

“…Several different computations have been attributed to synaptic depression, particularly in synapses where depression represents a single dominant form of STP Chance et al, 1998;Chung et al, 2002;Cook et al, 2003). The contributions of various STP components to synaptic computations have been more difficult to determine in synapses expressing multiple overlapping and interacting forms of STP (MacLeod et al, 2007). We used our modeling approach to examine the roles of STP components in synaptic dynamics based on elimination analysis (Fig.…”

Target-specific regulation of presynaptic release properties at auditory nerve terminals in the avian cochlear nucleus

“…In the avian auditory brain stem, a series of comparative studies have investigated the mechanisms that underlie STP, revealing a number of similarities and a few differences. Recovery from depression had similar biexponential times courses in both avian cochlear nuclei (Brenowitz and Trussell 2001a;MacLeod et al 2007;MacLeod and Horiuchi 2011), suggesting common activity-dependent mechanisms that accelerate recovery rates or the presence of multiple vesicle pools with heterogeneous recovery kinetics. The recovery trajectories in the avian cochlear nuclei thus have similarities to recovery trajectories found in mammalian auditory brain stem and several other areas (Dittman et al 2000;Hallermann et al 2010;Wang and Kaczmarek 1998;Wang and Manis 2008;Wu and Borst 1999;Yang and Xu-Friedman 2008).…”

“…In NM the plasticity is dominated by short-term depression (Brenowitz and Trussell 2001a;Zhang and Trussell 1994), while in NA the plasticity is a balanced mixture of facilitation and depression (MacLeod et al 2007). In the mammalian cochlear nucleus, a similar distinction in STP profiles can be observed at nerve terminals onto the bushy cells and those onto stellate cells, which form analogous pathways to NM and NA, respectively (Cao et al 2008;Cao and Oertel 2010;Oleskevich and Walmsley 2002;Wang and Manis 2008;Yang and Xu-Friedman 2008).…”