Wide‐ranging frequency preferences of auditory midbrain neurons: Roles of membrane time constant and synaptic properties

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Abstract
Periodicity is a fundamental sound attribute. Its coding has been the subject of intensive research, most of which has focused on investigating how the periodicity of sounds is processed through the synaptic machinery in the brain. The extent to which the intrinsic properties of cells play in periodicity coding, particularly in the creation of selectivity to periodic signals, is not well understood. We performed in vitro whole‐cell patch recordings in the frog torus semicircularis to investigate each neuron’s intrinsic membrane properties as well as responses to sinusoidal current injected through the electrode and periodic stimulation of the ascending afferent. We found that: (i) toral neurons were heterogeneous, showing diverse biophysical phenotypes having distinct membrane characteristics, including membrane time constants (τ) and ionic channel compositions (Ih, Ikir, Ikv and INaP); (ii) a neuron’s τ was tightly correlated with its current‐evoked frequency preference (FP; range: 0.05–50 Hz); (iii) application of blockers for Ih, Ikir and Ikv (but not INaP) shifted the τ as well as the cell’s current‐evoked FP, suggesting that these ion channels contribute to the cell’s FP through regulation of τ; (iv) a neuron’s τ was also correlated with its afferent‐evoked FP (range: 10–300 pulses/s); and (v) the range of afferent‐evoked FP was approximately one order higher than the range of current‐evoked FPs, suggesting that both the cell’s intrinsic membrane and synaptic properties contribute to determining the afferent‐evoked cell‐specific FP (whose range matched those of cell‐specific responses to sound stimulation, e.g. selectivity to amplitude modulation rate).