scholarly journals Dynamics of a neuronal pacemaker in the weakly electric fish Apteronotus

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Aaron R. Shifman ◽  
Yiren Sun ◽  
Chloé M. Benoit ◽  
John E. Lewis
Keyword(s):  
Electric Fish ◽  
Electric Organ Discharge ◽  
Electric Organ ◽  
Weakly Electric Fish ◽  
Biophysical Model ◽  
Normal Brain ◽  
Pacemaker Cells ◽  
Temporal Precision ◽  
Oscillatory Dynamics ◽  
Weakly Electric

Abstract The precise timing of neuronal activity is critical for normal brain function. In weakly electric fish, the medullary pacemaker network (PN) sets the timing for an oscillating electric organ discharge (EOD) used for electric sensing. This network is the most precise biological oscillator known, with sub-microsecond variation in oscillator period. The PN consists of two principle sets of neurons, pacemaker and relay cells, that are connected by gap junctions and normally fire in synchrony, one-to-one with each EOD cycle. However, the degree of gap junctional connectivity between these cells appears insufficient to provide the population averaging required for the observed temporal precision of the EOD. This has led to the hypothesis that individual cells themselves fire with high precision, but little is known about the oscillatory dynamics of these pacemaker cells. As a first step towards testing this hypothesis, we have developed a biophysical model of a pacemaker neuron action potential based on experimental recordings. We validated the model by comparing the changes in oscillatory dynamics produced by different experimental manipulations. Our results suggest that this relatively simple model can capture a large range of channel dynamics exhibited by pacemaker cells, and will thus provide a basis for future work on network synchrony and precision.

scholarly journals Dynamics of a neuronal pacemaker in the weakly electric fish Apteronotus

2020 ◽  
Author(s):  
Aaron R. Shifman ◽  
Yiren Sun ◽  
Chloé M. Benoit ◽  
John E. Lewis
Keyword(s):  
Electric Fish ◽  
Weakly Electric Fish ◽  
Biophysical Model ◽  
Feeding Time ◽  
Normal Brain ◽  
Biological Clocks ◽  
Pacemaker Cells ◽  
Temporal Precision ◽  
Oscillatory Dynamics ◽  
Weakly Electric

AbstractThe precise timing of neuronal activity is critical for normal brain function. In weakly electric fish, the medullary pacemaker network (PN) sets the timing for an oscillating electric organ discharge (EOD) used for electric sensing. This network is the most precise biological oscillator known, with sub-microsecond variation in oscillator period. The PN consists of two principle sets of neurons, pacemaker and relay cells, that are connected by gap junctions and normally fire in synchrony, one-to-one with each EOD cycle. However, the degree of gap junctional connectivity between these cells appears insufficient to provide the population averaging required for the observed temporal precision of the EOD. This has led to the hypothesis that individual cells themselves fire with high precision, but little is known about the oscillatory dynamics of these pacemaker cells. To this end, we have developed a biophysical model of a pacemaker neuron action potential based on experimental recordings. We validated the model by comparing the changes in oscillatory dynamics produced by different experimental manipulations. Our results suggest that a relatively simple model captures the complex dynamics exhibited by pacemaker cells, and that these dynamics may enhance network synchrony and precision.Author summaryMany neural networks in the brain exhibit activity patterns which oscillate regularly in time. These oscillations, like a clock, can provide a precise sense of time, enabling drummers to maintain complex beat patterns and pets to anticipate “feeding time”. The exact mechanisms by which brain networks give rise to these biological clocks are not clear. The pacemaker network of weakly electric fish has the highest precision of all known biological clocks. In this study, we develop a detailed biophysical model of neurons in the pacemaker network. We then validate the model against experiments using a nonlinear dynamics approach. Our results show that pacemaker precision is due, at least in part, to how individual pacemaker cells generate their activity. This supports the idea that temporal precision in this network is not solely an emergent property of the network but also relies on the dynamics of individual neurons.

Precision of the Pacemaker Nucleus in a Weakly Electric Fish: Network Versus Cellular Influences

2000 ◽  
Vol 83 (2) ◽  
pp. 971-983 ◽  
Author(s):  
Katherine T. Moortgat ◽  
Theodore H. Bullock ◽  
Terrence J. Sejnowski
Keyword(s):  
Electric Fish ◽  
Electric Organ Discharge ◽  
Electric Organ ◽  
Spike Timing ◽  
Weakly Electric Fish ◽  
Pacemaker Cells ◽  
Relay Cell ◽  
Spike Timing Precision ◽  
Pacemaker Nucleus ◽  
Weakly Electric

We investigated the relative influence of cellular and network properties on the extreme spike timing precision observed in the medullary pacemaker nucleus (Pn) of the weakly electric fish Apteronotus leptorhynchus. Of all known biological rhythms, the electric organ discharge of this and related species is the most temporally precise, with a coefficient of variation (CV = standard deviation/mean period) of 2 × 10−4 and standard deviation (SD) of 0.12–1.0 μs. The timing of the electric organ discharge is commanded by neurons of the Pn, individual cells of which we show in an in vitro preparation to have only a slightly lesser degree of precision. Among the 100–150 Pn neurons, dye injection into a pacemaker cell resulted in dye coupling in one to five other pacemaker cells and one to three relay cells, consistent with previous results. Relay cell fills, however, showed profuse dendrites and contacts never seen before: relay cell dendrites dye-coupled to one to seven pacemaker and one to seven relay cells. Moderate (0.1–10 nA) intracellular current injection had no effect on a neuron's spiking period, and only slightly modulated its spike amplitude, but could reset the spike phase. In contrast, massive hyperpolarizing current injections (15–25 nA) could force the cell to skip spikes. The relative timing of subthreshold and full spikes suggested that at least some pacemaker cells are likely to be intrinsic oscillators. The relative amplitudes of the subthreshold and full spikes gave a lower bound to the gap junctional coupling coefficient of 0.01–0.08. Three drugs, called gap junction blockers for their mode of action in other preparations, caused immediate and substantial reduction in frequency, altered the phase lag between pairs of neurons, and later caused the spike amplitude to drop, without altering the spike timing precision. Thus we conclude that the high precision of the normal Pn rhythm does not require maximal gap junction conductances between neurons that have ordinary cellular precision. Rather, the spiking precision can be explained as an intrinsic cellular property while the gap junctions act to frequency- and phase-lock the network oscillations.

scholarly journals Electrical signalling of dominance in a wild population of electric fish

2010 ◽  
Vol 7 (2) ◽  
pp. 197-200 ◽  
Author(s):  
Vincent Fugère ◽  
Hernán Ortega ◽  
Rüdiger Krahe
Keyword(s):  
High Frequency ◽  
Electric Fish ◽  
Electric Organ Discharge ◽  
Low Frequency ◽  
Electric Organ ◽  
Weakly Electric Fish ◽  
Dominance Status ◽  
Strong Positive Relationship ◽  
Electrical Signalling ◽  
Weakly Electric

Animals often use signals to communicate their dominance status and avoid the costs of combat. We investigated whether the frequency of the electric organ discharge (EOD) of the weakly electric fish, Sternarchorhynchus sp., signals the dominance status of individuals. We correlated EOD frequency with body size and found a strong positive relationship. We then performed a competition experiment in which we found that higher frequency individuals were dominant over lower frequency ones. Finally, we conducted an electrical playback experiment and found that subjects more readily approached and attacked the stimulus electrodes when they played low-frequency signals than high-frequency ones. We propose that EOD frequency communicates dominance status in this gymnotiform species.

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