Input-Specific Organization of Intrinsic Excitability Expands Coding Capacity of Fast-Spiking Auditory Neurons

Heterogeneity of presynaptic input and postsynaptic intrinsic excitability are two major variables that regulate neuronal firing rates and patterns. Yet, little is known about how these variables interplay to diversify the fidelity of excitation-spike coupling. To investigate their reciprocal relationship, we took advantage of the one-to-one innervation of mature calyx of Held-principal neuron synapses at the medial nucleus of the trapezoid body (MNTB) in the auditory brainstem of male and female mice. Given that sustainability of synaptic drive is directly correlated with the morphological complexity of presynaptic calyces, we characterized the intrinsic excitability of postsynaptic neurons with morphologically identified inputs. We discovered that morphologically simple calyces (stalks and ≤10 swellings) providing weaker synaptic drive preferentially innervate principal neurons that exhibit lower stimulation-spike coupling fidelity and display phasic firing patterns, while neurons contacted by complex calyces (stalks and >20 swellings) providing stronger synaptic drive exhibit higher stimulation-spike coupling fidelity and are predominantly associated with tonic firing. Phasic and tonic firing neurons have similar action potential shape and composition of low-threshold Kv1 and high-threshold Kv3 potassium currents but display marked differences in their input resistance and resting potassium conductance. Our results support a model in which a postsynaptic gradient of leak potassium channel density complements the presynaptic morpho-functional continuum to create an extended dynamic range of MNTB outputs. This synergy expands the coding capacity within a single population of neurons and supports multiple streams of auditory processing.