Encoding of Sensory Signals Through Balanced Ionotropic Receptor Dynamics and Voltage Dependent Membrane Noise

Abstract

Encoding behaviorally relevant stimuli in a noisy background is critical for animals to survive in their natural environment. We identify core biophysical and synaptic mechanisms that permit the encoding of low frequency signals in pyramidal neurons of the weakly electric fish Apteronotus leptorhynchus, an animal that can accurately encode miniscule (0.1%) amplitude modulations of its self-generated electric field. We demonstrate that slow NMDA-R mediated EPSPs are able to summate over many interspike intervals of the primary electrosensory afferents (EAs), effectively eliminating the EA spike train serial correlations from the pyramidal cell input. This permits stimulus-evoked changes in EA spiking to be transmitted efficiently to downstream ELL pyramidal cells, where a dynamic balance of NMDA-R and GABA-A-R currents is critical for encoding low frequency signals. Interestingly, AMPA-R activity is depressed and plays a negligible role in the generation of action potentials; instead, cell intrinsic membrane noise implements voltage-dependent stochastic resonance to amplify weak sensory input and appears to drive a significant proportion of pyramidal cell spikes. Together, these mechanisms may be sufficient for the ELL to encode signals near the threshold of behavioral detection.