Analysis of excitatory and inhibitory neuron types in the inferior colliculus based on I_h properties

The inferior colliculus (IC) is a large midbrain nucleus that integrates inputs from many auditory brainstem and cortical structures. Despite its prominent role in auditory processing, the various cell types and their connections within the IC are not well characterized. To further separate GABAergic and non-GABAergic neuron types according to their physiological properties, we used a mouse model that expresses channelrhodopsin and enhanced yellow fluorescent protein in all GABAergic neurons and allows identification of GABAergic cells by light stimulation. Neuron types were classified upon electrophysiological measurements of the hyperpolarizing-activated current (I_h) in acute brain slices of young adult mice. All GABAergic neurons from our sample displayed slow-activating I_h with moderate amplitudes, whereas a subset of excitatory neurons showed fast-activating I_h with large amplitudes. This is in agreement with our finding that immunoreactivity against the fast-gating hyperpolarization-activated and cyclic-nucleotide-gated 1 (HCN1) channel was present around excitatory neurons, whereas the slow-gating HCN4 channel was found perisomatically around most inhibitory neurons. I_h properties and neurotransmitter types were correlated with firing patterns to depolarizing current pulses. All GABAergic neurons displayed adapting firing patterns very similar to the majority of glutamatergic neurons. About 15% of the glutamatergic neurons showed an onset spiking pattern, always in combination with large and fast I_h. We conclude that HCN channel subtypes are differentially distributed in IC neuron types and correlate with neurotransmitter type and firing pattern. In contrast to many other brain regions, membrane properties and firing patterns were similar in GABAergic neurons and about one-third of the excitatory neurons. NEW & NOTEWORTHY Neuron types in the central nucleus of the auditory midbrain are not well characterized regarding their transmitter type, ion channel composition, and firing pattern. The present study shows that GABAergic neurons have slowly activating hyperpolarizing-activated current (I_h) and an adaptive firing pattern whereas at least four types of glutamatergic neurons exist regarding their I_h properties and firing patterns. Many of the glutamatergic neurons were almost indistinguishable from the GABAergic neurons regarding I_h properties and firing pattern.