Aims: SCA13 patients exhibit an extracerebellar auditory phenotype characterized by sound localization deficits, despite normal audiograms. This phenotype is caused by the R420H point mutation in the KCNC3 gene which encodes for Kv3.3 subunits of high-voltage gated potassium channels. Here, we investigate how this mutation leads to disruption of temporal processing along the auditory pathway.Methods: The R420H mouse model was created using CRISPR-Cas9. Whole-cell patch-clamp electrophysiology and afferent synaptic stimulation in acute mouse brain slices were used to characterize neural firing properties of affected auditory neurons. Degrees of neurodegeneration were assessed via cell number, cell size, p62/cleaved caspase expression and subcellular distribution of Kv3.3.Results: In contrast to cerebellar Purkinje neurons, auditory brainstem neurons survive in age-matched SCA13 mice. Action potential (AP) half-widths of lateral superior olive (LSO) neurons increased in duration by around 2–3 fold. Recovery from refractory periods between APs were insufficient and this prevented the characteristic high-frequency AP following in response to synaptic train inputs. Co-immunolabelling of Kv3.3 protein with the vesicular glutamate transporter protein (VGluT1) and neuronal glycine transporter protein (GlyT2) indicated expression of Kv3.3 in excitatory and inhibitory synapses, respectively.Conclusions: The largely prolonged AP duration in LSO neurons disrupts high-frequency firing which likely contributes the sound localization deficits observed in the human kindred of SCA13. The survival of LSO neurons in 6-month old homozygote mice are in stark contrast to the loss of Purkinje neurons in the same mice and may provide a target to investigate neuroprotective mechanisms in degenerative disease models.