Transient Signals Trigger Synchronous Bursts in an Identified Population of Neurons

Abstract

It is an important task in neuroscience to find general principles that relate neural codes to the structure of the signals they encode. The structure of sensory signals can be described in many ways, but one important categorization distinguishes continuous from transient signals. We used the communication signals of the weakly electric fish to reveal how transient signals (chirps) can be easily distinguished from the continuous signal they disrupt. These communication signals-low-frequency sinusoids interrupted by high-frequency transients-were presented to pyramidal cells of the electrosensory lateral line lobe (ELL) during in vivo recordings. We show that a specific population of electrosensory neurons encodes the occurrence of the transient signal by synchronously producing a burst of spikes, whereas bursting was neither common nor synchronous in response to the continuous signal. We also confirmed that burst can be triggered by low-frequency modulations typical of prey signals. However, these bursts are more common in a different segment of the ELL and during spatially localized stimulation. These localized stimuli will elicit synchronized bursting only in a restricted number of cells the receptive fields of which overlap the spatial extent of the stimulus. Therefore the number of cells simultaneously producing a burst and the ELL segment responding most strongly may carry the information required to disambiguate chirps from prey signals. Finally we show that the burst response to chirps is due to a biophysical mechanism previously characterized by in vitro studies of electrosensory neurons. We conclude that bursting and synchrony across cells are important mechanisms used by sensory neurons to carry the information about behaviorally relevant but transient signals.

In vivo conditions influence the coding of stimulus features by bursts of action potentials

“…We nevertheless note that bursts from ELL pyramidal cells appear to be a behaviorally relevant signal as midbrain neurons that receive direct synaptic input from ELL pyramidal cells respond selectively to these (Fortune and Rose 1997). This is supported by recent studies showing that ELL pyramidal neurons respond to communication stimuli with bursts of action potentials (Marsat et al 2009;Marsat and Maler 2010). Further studies are needed to investigate potential correlations between burst and communication stimuli attributes and their role in mediating behavior.…”

Burst-Induced Anti-Hebbian Depression Acts through Short-Term Synaptic Dynamics to Cancel Redundant Sensory Signals

“…As described below, this protocol failed to induce any form of plasticity. Given our previous work demonstrating the role of spike bursts in encoding low-frequency electrosensory signals (Oswald et al, 2004(Oswald et al, , 2007Ellis et al, 2007;Mehaffey et al, 2008;Marsat et al, 2009), we then used a variety of presynaptic and postsynaptic burst-pairing protocols in order to determine which, if any, might be capable of inducing longterm synaptic plasticity. In addition, we also investigated whether the induced plasticity was specific to the stimulated synapses.…”

“…The requirement for postsynaptic bursts provides a direct link with natural spike patterns that occur during adaptive cancellation. Spike bursts in the CLS and CMS code specifically for low-frequency signals (Oswald et al, 2004) (Marsat et al, 2009). Burst discharge is initiated by the depolarizing afterpotentials (DAPs) that follow back-propagation of spikes up the SPC's apical dendritic tree Section (Turner et al, 2002); bursts are therefore also associated with depolarization of the dendritic targets of PF feedback.…”

“…Delay times are as follows: Ϯ5, Ϯ10, Ϯ20, Ϯ30, and Ϯ100 ms. Error bars show the SD in C, E, and F. tentials (DAPs) that, in turn, are due to somatic spikes backpropagating into their apical dendrites (Turner et al, 1994(Turner et al, , 1996. In the centrolateral ELL and centromedial segments (CMS) bursts code for low-frequency prey-like sensory signals, whereas isolated spikes can encode high-frequency global communication-like signals (Oswald et al, 2004(Oswald et al, , 2007Ellis et al, 2007;Mehaffey et al, 2008;Marsat et al, 2009). Further, lowfrequency input to a pyramidal cell's RF induces bursting Marsat et al, 2009).…”

“…In the centrolateral ELL and centromedial segments (CMS) bursts code for low-frequency prey-like sensory signals, whereas isolated spikes can encode high-frequency global communication-like signals (Oswald et al, 2004(Oswald et al, , 2007Ellis et al, 2007;Mehaffey et al, 2008;Marsat et al, 2009). Further, lowfrequency input to a pyramidal cell's RF induces bursting Marsat et al, 2009). Cancellation of this signal requires low-frequency spatially diffuse (global) activation of the pyramidal cell's nonclassic RF (Chacron et al, 2003), and this is conveyed by the indirect cerebellar (EGp) PF feedback pathway to their apical dendrites .…”