Enhancement of Signal-to-Noise Ratio and Phase Locking for Small Inputs by a Low-Threshold Outward Current in Auditory Neurons

Abstract

Neurons possess multiple voltage-dependent conductances specific for their function. To investigate how low-threshold outward currents improve the detection of small signals in a noisy background, we recorded from gerbil medial superior olivary (MSO) neurons in vitro. MSO neurons responded phasically, with a single spike to a step current injection. When bathed in dendrotoxin (DTX), most cells switched to tonic firing, suggesting that low-threshold potassium currents (I(KLT)) participated in shaping these phasic responses. Neurons were stimulated with a computer-generated steady barrage of random inputs, mimicking weak synaptic conductance transients (the "noise"), together with a larger but still subthreshold postsynaptic conductance, EPSG (the "signal"). DTX reduced the signal-to-noise ratio (SNR), defined as the ratio of probability to fire in response to the EPSG and the probability to fire spontaneously in response to noise. The reduction was mainly attributable to the increase of spontaneous firing in DTX. The spike-triggered reverse correlation indicated that, for spike generation, the neuron with I(KLT) required faster inward current transients. This narrow temporal integration window contributed to superior phase locking of firing to periodic stimuli before application of DTX. A computer model including Hodgkin-Huxley type conductances for spike generation and for I(KLT) (Rathouz and Trussell, 1998) showed similar response statistics. The dynamic low-threshold outward current increased SNR and the temporal precision of integration of weak subthreshold signals in auditory neurons by suppressing false positives.

Influence of subthreshold nonlinearities on signal-to-noise ratio and timing precision for small signals in neurons: minimal model analysis

“…Previously, we studied experimentally (gerbil, in vitro slice preparation) how SNR and phase-locking are affected by low-threshold potassium currents in MSO neurons (Svirskis et al 2002), finding results similar to those in this paper. We also showed there using a Hodgkin-Huxley type model that a low-threshold potassium conductance, based on experimentally defined parameters, could account for the effects observed.…”

“…We also showed there using a Hodgkin-Huxley type model that a low-threshold potassium conductance, based on experimentally defined parameters, could account for the effects observed. In this work, we used the LIF model enhanced with a time-dependent piecewise-linear membrane currentvoltage relation and showed that its response properties were qualitatively similar to those recorded experimentally and seen in a model with Hodgkin-Huxley type conductances (Svirskis et al 2002). This means that the minimal model captures a number of the essential firing and membrane properties of phasic auditory neurons.…”

“…Although it may be that some optimal noise strength can maximize the effects of negative feedback, this remains to be explored in future studies. In our previous work using a conductance-based spiking model (Svirskis et al 2002) we saw that the probability of firing in response to the `signal' EPSC decreased for low and high levels of noise.…”

“…We recently explored these issues for MSO neurons both experimentally (gerbil, in vitro) and computationally with a Hodgkin-Huxley model that included I KLT (Svirskis et al 2002).…”

Modeling coincidence detection in nucleus laminaris

“…In addition to those models of NL referred to above, there are related models of coincidence detection in mammalian medial superior olive (MSO), or models general enough to apply equally well to both MSO and NL (Colburn et al 1990;Han and Colburn 1993;Brughera et al 1995;Brand et al 2002;Colburn and Zhou 2002;Svirskis et al 2002;Svirskis and Rinzel 2003;Zhou and Colburn 2003). For a dated but valuable review, see Colburn (1996).…”