Abstract
Neuronal membrane properties can largely vary even within distinct morphological cell classes. The mechanisms and functional consequences of this diversity, however, are little explored. In the medial superior olive (MSO), a brainstem nucleus that performs binaural coincidence detection, membrane properties at rest are largely governed by the hyperpolarization-activated inward current (Ih) which enables the temporally precise integration of excitatory and inhibitory inputs. Here, we report that Ih density varies along the putative tonotopic axis of the MSO with Ih being largest in ventral, high-frequency (HF) processing neurons. Also Ih half-maximal activation voltage and time constant are differentially distributed such that Ih of the putative HF processing neurons activate faster and at more depolarized levels. Intracellular application of saturating concentrations of cyclic AMP removed the regional difference in hyperpolarization-activated cyclic nucleotide gated (HCN) channel activation, but not Ih density. Experimental data in conjunction with a computational model suggest that increased Ih levels are helpful in counteracting temporal summation of phase-locked inhibitory inputs which is particularly prominent in HF neurons.
Highlights
Neuronal encoding of information in the time domain is enhanced by specific adjustments of membrane properties to the dynamics and temporal characteristics of the inputs (O’Donnell and Nolan, 2011)
In the present study we demonstrate that Ih amplitude systematically varies along the dorsoventral axis of the medial superior olive (MSO), being largest in ventral neurons and smallest in dorsal neurons
Consistent with this dorsoventral organization of membrane properties, the integration of inhibitory inputs systematically varies as a function of the neuron’s location in both experiments and the model indicating that MSO neurons are tuned differentially along the presumed tonotopic axis
Summary
Neuronal encoding of information in the time domain is enhanced by specific adjustments of membrane properties to the dynamics and temporal characteristics of the inputs (O’Donnell and Nolan, 2011) This is especially important for neurons in the medial superior olive (MSO), a binaural nucleus in the auditory brainstem that analyses interaural time differences (ITDs) of different input frequencies with extremely high temporal precision. Important for the high temporal precision with which these neurons integrate their excitatory and inhibitory inputs are the large voltage-gated channels that are open around the resting potential of the membrane Such exquisitely fine-tuned temporal processing crucially depends on the composition and the properties of voltage-gated ion channels. We explored the putative functional consequences of this relationship theoretically using a computational singlecompartment model featuring HCN and KLVA channels that was fitted to electrophysiological recordings: this model suggests that integration of inhibitory inputs in a frequency-dependent manner helps to maintain the neuron’s membrane potential close to firing threshold
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