Ghostbursting: A Novel Neuronal Burst Mechanism

Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Ontario, Canada
Journal of Computational Neuroscience (Impact Factor: 1.74). 01/2002; 12(1):5-25. DOI: 10.1023/A:1014921628797
Source: PubMed


Pyramidal cells in the electrosensory lateral line lobe (ELL) of weakly electric fish have been observed to produce high-frequency burst discharge with constant depolarizing current (Turner et al., 1994). We present a two-compartment model of an ELL pyramidal cell that produces burst discharges similar to those seen in experiments. The burst mechanism involves a slowly changing interaction between the somatic and dendritic action potentials. Burst termination occurs when the trajectory of the system is reinjected in phase space near the "ghost" of a saddle-node bifurcation of fixed points. The burst trajectory reinjection is studied using quasi-static bifurcation theory, that shows a period doubling transition in the fast subsystem as the cause of burst termination. As the applied depolarization is increased, the model exhibits first resting, then tonic firing, and finally chaotic bursting behavior, in contrast with many other burst models. The transition between tonic firing and burst firing is due to a saddle-node bifurcation of limit cycles. Analysis of this bifurcation shows that the route to chaos in these neurons is type I intermittency, and we present experimental analysis of ELL pyramidal cell burst trains that support this model prediction. By varying parameters in a way that changes the positions of both saddle-node bifurcations in parameter space, we produce a wide gallery of burst patterns, which span a significant range of burst time scales.

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Available from: Andre Longtin
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    • "Our pyramidal cell model contains two compartments and reproduces the main features of ELL pyramidal cell burst firing seen in vitro (Doiron et al. 2002; Oswald et al. 2004; Doiron et al. 2007). The model consists of somatic and dendritic compartments connected through an axial resistance of 1/g c (g c : coupling conductance). "
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    ABSTRACT: The functional role of burst firing (i.e. the firing of packets of action potentials followed by quiescence) in sensory processing is still under debate. Should bursts be considered as unitary events that signal the presence of a particular feature in the sensory environment or is information about stimulus attributes contained within their temporal structure? We compared the coding of stimulus attributes by bursts in vivo and in vitro of electrosensory pyramidal neurons in weakly electric fish by computing correlations between burst and stimulus attributes. Our results show that, while these correlations were strong in magnitude and significant in vitro, they were actually much weaker in magnitude if at all significant in vivo. We used a mathematical model of pyramidal neuron activity in vivo and showed that such a model could reproduce the correlations seen in vitro, thereby suggesting that differences in burst coding were not due to differences in bursting seen in vivo and in vitro. We next tested whether variability in the baseline (i.e. without stimulation) activity of ELL pyramidal neurons could account for these differences. To do so, we injected noise into our model whose intensity was calibrated to mimic baseline activity variability as quantified by the coefficient of variation. We found that this noise caused significant decreases in the magnitude of correlations between burst and stimulus attributes and could account for differences between in vitro and in vivo conditions. We then tested this prediction experimentally by directly injecting noise in vitro through the recording electrode. Our results show that this caused a lowering in magnitude of the correlations between burst and stimulus attributes in vitro and gave rise to values that were quantitatively similar to those seen under in vivo conditions. While it is expected that noise in the form of baseline activity variability will lower correlations between burst and stimulus attributes, our results show that such variability can account for differences seen in vivo. Thus, the high variability seen under in vivo conditions has profound consequences on the coding of information by bursts in ELL pyramidal neurons. In particular, our results support the viewpoint that bursts serve as a detector of particular stimulus features but do not carry detailed information about such features in their structure.
    Full-text · Article · Oct 2011 · Journal of Computational Neuroscience
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    • "Anatomical studies have furthermore shown large differences in the distributions of several ion channels and ligand-gated ionotropic receptors between deep and superficial pyramidal cells such as NMDA receptors (Harvey- Girard and Dunn, 2003; Harvey-Girard et al., 2007), small conductance (SK) calcium-activated potassium channels (Ellis et al., 2007b, 2008), and IP3 receptors (Berman et al., 1995). ELL pyramidal cells also display an intrinsic burst mechanism that has been well characterized in vitro and relies on a somatodendritic interaction (Lemon and Turner, 2000; Doiron et al., 2001, 2002, 2003b; Noonan et al., 2003; Fernandez et al., 2005; Mehaffey et al., 2008a): somatic action potentials backpropagate into the apical dendritic tree where they cause a dendritic action potential that propagates back to the soma, leading to a depolarizing afterpotential (DAP) which can cause another somatic action potential. The strength of the DAP grows throughout the burst, leading to a shortening of the interspike interval. "
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    ABSTRACT: Many neurons tend to fire clusters of action potentials called bursts followed by quiescence in response to sensory input. While the mechanisms that underlie burst firing are generally well understood in vitro, the functional role of these bursts in generating behavioral responses to sensory input in vivo are less clear. Pyramidal cells within the electrosensory lateral line lobe (ELL) of weakly electric fish offer an attractive model system for studying the coding properties of burst firing, because the anatomy and physiology of the electrosensory circuitry are well understood, and the burst mechanism of ELL pyramidal cells has been thoroughly characterized in vitro. We investigated the coding properties of bursts generated by these cells in vivo in response to mimics of behaviorally relevant sensory input. We found that heterogeneities within the pyramidal cell population had quantitative but not qualitative effects on burst coding for the low frequency components of broadband time varying input. Moreover, spatially localized stimuli mimicking, for example, prey tended to elicit more bursts than spatially global stimuli mimicking conspecific-related stimuli. We also found small but significant correlations between burst attributes such as the number of spikes per burst or the interspike interval during the burst and stimulus attributes such as stimulus amplitude or slope. These correlations were much weaker in magnitude than those observed in vitro. More surprisingly, our results show that correlations between burst and stimulus attributes actually decreased in magnitude when we used low frequency stimuli that are expected to promote burst firing. We propose that this discrepancy is attributable to differences between ELL pyramidal cell burst firing under in vivo and in vitro conditions.
    Full-text · Article · Mar 2010 · Neuroscience
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    • "We added both synaptic input and SK currents to the dendritic compartments of both models, with the synaptic current providing a source of Ca 2ϩ to the dendrite, thereby activating dendritic SK channels as detailed in METHODS. With the synaptic conductance g max ϭ 0, the large compartmental model produced bursting similar to that seen in vitro that terminated with dendritic failures (Doiron et al. 2001b, 2002) (Fig. 8A). Adding the synaptic input (g max ϭ 6 ϫ 10 "
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    ABSTRACT: Understanding the mechanistic substrates of neural computations that lead to behavior remains a fundamental problem in neuroscience. In particular, the contributions of intrinsic neural properties such as burst firing and dendritic morphology to the processing of behaviorally relevant sensory input have received much interest recently. Pyramidal cells within the electrosensory lateral line lobe of weakly electric fish display an intrinsic bursting mechanism that relies on somato-dendritic interactions when recorded in vitro: backpropagating somatic action potentials trigger dendritic action potentials that lead to a depolarizing afterpotential (DAP) at the soma. We recorded intracellularly from these neurons in vivo and found firing patterns that were quite different from those seen in vitro: we found no evidence for DAPs as each somatic action potential was followed by a pronounced afterhyperpolarization (AHP). Calcium chelators injected in vivo reduced the AHP, thereby unmasking the DAP and inducing in vitro-like bursting in pyramidal cells. These bursting dynamics significantly reduced the cell's ability to encode the detailed time course of sensory input. We performed additional in vivo pharmacological manipulations and mathematical modeling to show that calcium influx through N-methyl-d-aspartate (NMDA) receptors activate dendritic small conductance (SK) calcium-activated potassium channels, which causes an AHP that counteracts the DAP and leads to early termination of the burst. Our results show that ion channels located in dendrites can have a profound influence on the processing of sensory input by neurons in vivo through the modulation of an intrinsic bursting mechanism.
    Full-text · Article · Sep 2009 · Journal of Neurophysiology
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