Sensory coding in oscillatory electroreceptors of paddlefish

Abstract

Coherence and information theoretic analyses were applied to quantitate the response properties and the encoding of time-varying stimuli in paddlefish electroreceptors (ERs), studied in vivo. External electrical stimuli were Gaussian noise waveforms of varied frequency band and strength, including naturalistic waveforms derived from zooplankton prey. Our coherence analyses elucidated the role of internal oscillations and transduction processes in shaping the 0.5-20 Hz best frequency tuning of these electroreceptors, to match the electrical signals emitted by zooplankton prey. Stimulus-response coherence fell off above approximately 20 Hz, apparently due to intrinsic limits of transduction, but was detectable up to 40-50 Hz. Aligned with this upper fall off was a narrow band of intense internal noise at ∼25 Hz, due to prominent membrane potential oscillations in cells of sensory epithelia, which caused a narrow deadband of external insensitivity. Using coherence analysis, we showed that more than 76% of naturalistic stimuli of weak strength, ∼1 μV∕cm, was linearly encoded into an afferent spike train, which transmitted information at a rate of ∼30 bits∕s. Stimulus transfer to afferent spike timing became essentially nonlinear as the stimulus strength was increased to induce bursting firing. Strong stimuli, as from nearby zooplankton prey, acted to synchronize the bursting responses of afferents, including across populations of electroreceptors, providing a plausible mechanism for reliable information transfer to higher-order neurons through noisy synapses.