Abstract
A high-frequency, subthreshold resonance in the guinea pig medial superior olive (MSO) was recently linked to the efficient extraction of spatial cues from the fine structure of acoustic stimuli. We report here that MSO neurons in gerbil also have resonant properties and, based on our whole-cell recordings and computational modeling, that a low-voltage-gated potassium current, IKLT, underlies the resonance. We show that resonance was lost following dynamic clamp replacement of IKLT with a leak conductance and in the model when voltage-gating of IKLT was suppressed. Resonance was characterized using small amplitude sinusoidal stimuli to generate impedance curves as typically done for linear systems analysis. Extending our study into the nonlinear, voltage-dependent regime, we increased stimulus amplitude and found, experimentally and in simulations, that the subthreshold resonant frequency (242Hz for weak stimuli) increased continuously to the resonant frequency for spiking (285Hz). The spike resonance of these phasic-firing (type III excitable) MSO neurons and of the model is of particular interest also because previous studies of resonance typically involved neurons/models (type II excitable, such as the standard Hodgkin-Huxley model) that can fire tonically for steady inputs. To probe more directly how these resonances relate to MSO neurons as slope-detectors, we presented periodic trains of brief, fast-rising excitatory post-synaptic potentials (EPSCs) to the model. While weak subthreshold EPSC trains were essentially low-pass filtered, resonance emerged as EPSC amplitude increased. Interestingly, for spike-evoking EPSC trains, the threshold amplitude at spike resonant frequency (317Hz) was lower than the single ESPC threshold. Our finding of a frequency-dependent threshold for repetitive brief EPSC stimuli and preferred frequency for spiking calls for further consideration of both subthreshold and suprathreshold resonance to fast and precise temporal processing in the MSO.
Highlights
The intrinsic frequency preference of neurons for oscillatory inputs, otherwise known as subthreshold resonance, has been associated with the efficient extraction of auditory information
Principal neurons of the medial superior olive (MSO) are fast and precise coincidence detectors involved in the neuronal computation of sound localization
We used electrophysiological recordings and computational modelling to identify the key biophysical factors for this fast resonance: a low-threshold potassium current, IKLT, whose activation time constant is slightly slower than the membrane time constant
Summary
The intrinsic frequency preference of neurons for oscillatory inputs, otherwise known as subthreshold resonance, has been associated with the efficient extraction of auditory information. Principal neurons of the guinea pig medial superior olive (MSO) display an intrinsic preference for subthreshold, sinusoidal stimuli between 80-400Hz [4]. While the fast passive properties are well characterized, there is less certainty about the ‘resonant’ current Remme et al [4] did highlight the low-threshold, voltage-gated potassium current, IKLT, as being an ideal candidate This outward current provides negative feedback to depolarizing currents and possesses suitable activation gating properties (time constant % 1ms) and is present in high densities throughout an MSO neuron [14]. Experimental data from the mesencephalic nerve and computational evidence in the nucleus laminaris (the avian analogue of the mammalian MSO) point to IKLT underlying similar high-frequency subthreshold resonances (>80Hz) [15,16]
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