Spike-Interval Triggered Averaging Reveals a Quasi-Periodic Spiking Alternative for Stochastic Resonance in Catfish Electroreceptors

Abstract

Catfish detect and identify invisible prey by sensing their ultra-weak electric fields with electroreceptors. Any neuron that deals with small-amplitude input has to overcome sensitivity limitations arising from inherent threshold non-linearities in spike-generation mechanisms. Many sensory cells solve this issue with stochastic resonance, in which a moderate amount of intrinsic noise causes irregular spontaneous spiking activity with a probability that is modulated by the input signal. Here we show that catfish electroreceptors have adopted a fundamentally different strategy. Using a reverse correlation technique in which we take spike interval durations into account, we show that the electroreceptors generate a supra-threshold bias current that results in quasi-periodically produced spikes. In this regime stimuli modulate the interval between successive spikes rather than the instantaneous probability for a spike. This alternative for stochastic resonance combines threshold-free sensitivity for weak stimuli with similar sensitivity for excitations and inhibitions based on single interspike intervals.

Frequency-dependent avoidance movement of glass catfish in response to sinusoidal electrical stimulation and associated spiking patterns of electroreceptors

“…Sinusoidal electrical stimulation to glass catfish shortens the interspike interval (ISI) in one half period and prolongs the ISI in the other half ( Bretschneider et al, 1985 ). Bursting patterns are considered to contribute to reliable signal transmission ( Izhikevich et al, 2003 ) and are often found in electroreceptors and their associated cells ( Wilkens et al, 1997 ; Neiman and Russell, 2002 ; Oswald et al, 2004 ; Lankheet et al, 2012 ). Daphnia or Ornstein-Uhlenbeck Gaussian noise induce bursting in the electroreceptors of paddle fish ( Wilkens et al, 1997 ; Neiman and Russell, 2002 ).…”

Optimal stimulus waveforms for eliciting a spike: How close is the spike-triggered average?

“…For nearly half a century, spike-triggered averaging (STA) has been used in experimental neuroscience to gain insight into neuronal responses to stimulus features [1]–[6]. STA using broadband stochastic stimulation has revealed mechanisms that govern how inherently noisy sensory information might be encoded by neurons.…”