Abstract
Principal neurons of the lateral superior olivary nucleus (LSO) respond selectively to interaural level differences (ILD). To perform this computation, LSO neurons integrate excitatory synaptic drive from the ipsilateral ear with inhibitory synaptic drive from the contralateral ear via the medial nucleus of the trapezoid body (MNTB). Previous research demonstrated that inhibitory terminals from the MNTB to the LSO are eliminated during development. Furthermore, MNTB synapses display an activity- and age-dependent long-term depression (iLTD) that may contribute to inhibitory synapse elimination. However, inhibitory synapses that are stabilized become stronger. Here, we asked whether MNTB synapses displayed activity-dependent strengthening. Whole-cell recordings were obtained from LSO neurons in a gerbil brain slice before and after hearing onset. The inhibitory MNTB afferents were stimulated at a low rate, similar to spontaneous discharge rates observed in vivo. The MNTB-evoked inhibitory responses were strengthened by 40–300% when synaptic activity was coupled with postsynaptic membrane depolarization, exogenous glutamate application, or activation of ipsilateral excitatory synaptic inputs. This inhibitory long-term potentiation (iLTP) was associated with increased spontaneous inhibitory postsynaptic current (IPSC) amplitude and frequency. One hour after iLTP induction, IPSCs could not be de-potentiated by the MNTB stimulation pattern that induces iLTD in control slices. iLTP could only be induced after hearing onset (>P12), and was blocked in the presence of a GABAB receptor antagonist. Together, these results suggest a developmental period during which the induction of iLTP depends on the conjoint activation of GABAB receptors and postsynaptic depolarization. We propose that iLTP may support stabilization of un-pruned MNTB connections and contribute to the emergence of ILD processing in the mature LSO.
Highlights
The encoding of sound localization cues, such as interaural level (ILD) and time differences (ITD), begins in the ventral auditory brain stem
For interaural level differences (ILD) coding, the discharge rate of lateral superior olivary (LSO) neurons is proportional to the integration of ipsilateral excitatory drive arising from the cochlear nucleus and contralateral inhibitory drive from the medial nucleus of the trapezoid body (MNTB) (Boudreau and Tsutchitani, 1968; Caird and Klinke, 1983; Harnischfeger et al, 1985; Tollin, 2003; Sterenborg et al, 2010)
The major finding of this study is that inhibitory MNTB synapses onto the LSO display an activity-dependent long-term potentiation following hearing onset (P12) but not prior to that
Summary
The encoding of sound localization cues, such as interaural level (ILD) and time differences (ITD), begins in the ventral auditory brain stem. A similar elimination of inhibitory MNTB terminals occurs at the medial superior olivary nucleus, which encodes ITD (Kapfer et al, 2002), one study did not find a significant developmental change in amplitude (Walcher et al, 2011). It is, plausible that that the establishment of properly aligned excitatory and inhibitory maps involves the dynamic addition and elimination of inhibitory synapses. We describe a mechanism that could account for this strengthening
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