To Burst or Not to Burst?

Abstract

It is well known that some neurons tend to fire packets of action potentials followed by periods of quiescence (bursts) while others within the same stage of sensory processing fire in a tonic manner. However, the respective computational advantages of bursting and tonic neurons for encoding time varying signals largely remain a mystery. Weakly electric fish use cutaneous electroreceptors to convey information about sensory stimuli and it has been shown that some electroreceptors exhibit bursting dynamics while others do not. In this study, we compare the neural coding capabilities of tonically firing and bursting electroreceptor model neurons using information theoretic measures. We find that both bursting and tonically firing model neurons efficiently transmit information about the stimulus. However, the decoding mechanisms that must be used for each differ greatly: a non-linear decoder would be required to extract all the available information transmitted by the bursting model neuron whereas a linear one might suffice for the tonically firing model neuron. Further investigations using stimulus reconstruction techniques reveal that, unlike the tonically firing model neuron, the bursting model neuron does not encode the detailed time course of the stimulus. A novel measure of feature detection reveals that the bursting neuron signals certain stimulus features. Finally, we show that feature extraction and stimulus estimation are mutually exclusive computations occurring in bursting and tonically firing model neurons, respectively. Our results therefore suggest that stimulus estimation and feature extraction might be parallel computations in certain sensory systems rather than being sequential as has been previously proposed.

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

“…This current decays exponentially with time constant τ b and is incremented by a fixed amount ΔI b after a time delay d following each spike time t i . We note that a full biophysical justification of this current and of the model in general can be found in (Chacron et al, 2001a,b;Chacron et al, 2004). Previous studies have also shown that this model could reproduce experimental data from electroreceptor afferents with good accuracy (Chacron et al, 2001a(Chacron et al, ,b, 2004.…”

“…6A). Previous studies have provided a full biophysical justification for this model and have shown that it can reproduce both the experimentally observed heterogeneities in the baseline firing statistics of primary electrosensory afferents (Chacron et al, 2000(Chacron et al, , 2001b(Chacron et al, , 2004 as well as the experimentally observed responses to sensory input (Chacron et al, 2005b;Chacron, 2006). We first applied AM stimuli to the model and found that it could qualitatively reproduce the results seen experimentally.…”

“…In order to gain greater understanding as to what causes a neuron to respond to the envelope, we used a previously described leaky integrate and fire model with dynamic threshold (LIFDT) (Chacron et al, 2000(Chacron et al, , 2001a(Chacron et al, , 2003b) with a burst current (Chacron et al, 2001b(Chacron et al, , 2004). The model is described by the following differential equations:…”

“…The rectification values were defined as the percent of bins for which the count was less than 30% of the mean bin count. Table 1 Parameter values used in numerical simulations of our model are similar to those used in previous studies (Chacron et al, 2001b(Chacron et al, , 2004 Correlation coefficients between the baseline firing rate and the maximum of the envelope-response coherence obtained for the different stimulus frequency ranges and contrasts used in this study …”

A Behavioral Role for Feature Detection by Sensory Bursts

“…Bursts occur in a number of sensory systems (Eggermount and Smith, 1996;Yu and Margoliash, 1996;Sherman, 2001;Martinez-Conde et al, 2002;Chacron et al, 2004;Krahe and Gabbiani, 2004), and it has been proposed that they constitute a specific neural code, signaling the occurrence of behaviorally relevant sensory events. The possible coding functions of sensory bursts have been studied particularly thoroughly in the lateral geniculate nucleus (LGN) of mammals and in the electrosensory lateral line lobe (ELL) of weakly electric fish.…”