Ultrafast traveling wave dominates the electric organ discharge of Apteronotus leptorhynchus: an inverse modelling study

Abstract

Identifying and understanding the current sources that give rise to bioelectric fields is a fundamental problem in the biological sciences. It is very difficult, for example, to attribute the time-varying features of an electroencephalogram recorded from the head surface to the neural activity of specific brain areas; model systems can provide important insight into such problems. Some species of fish actively generate an oscillating (c. 1000 Hz) quasi-dipole electric field to communicate and sense their environment in the dark. A specialized electric organ comprises neuron-like cells whose collective signal underlies this electric field. As a step towards understanding the detailed biophysics of signal generation in these fish, we use an anatomically-detailed finite-element modelling approach to reverse-engineer the electric organ signal over one oscillation cycle. We find that the spatiotemporal profile of current along the electric organ constitutes a travelling wave that is well-described by two spatial Fourier components varying in time. The conduction velocity of this wave is faster than action potential conduction in any known neuronal axon (>200 m/s), suggesting that the spatiotemporal features of high-frequency electric organ discharges are not constrained by the conduction velocities of spinal neuron pathways.

The complexity of high-frequency electric fields degrades electrosensory inputs: implications for the jamming avoidance response in weakly electric fish

“…We perform a detailed comparison of the spatio-temporal features of jamming signals between Eigenmannia and Apteronotus using computational models. We have previously developed a model for the time varying electric field of a 21 cm long Apteronotus leptorhynchus [26], and describe here a similar model for Eigenmannia. In brief, a two-dimensional cross section of the Eigenmannia body (26 cm in length) was divided into three compartments: skin, body and electric organ.…”

“…The skin comprised a 100 mm layer and the electric organ was defined as a 0.01 Â 22 cm rectangle centred about the rostro-caudal axis and beginning 3 cm from the tip of the nose. The electrical conductivities for each body compartment were taken from the Apteronotus model [26,31]. To replicate the experimental recording conditions, the fish model was placed in a 70 Â 70 cm 'tank' with water conductivity of 200 mS cm 21 [27,32], and a reference (ground) electrode in the corner of the tank nearest the head.…”

“…In previous work, we developed a finite-element model of the spatio-temporal electric field generated by Apteronotus [26]. To compare the electric signals available for sensing by Eigenmannia and Apteronotus, we developed a similar model of the Eigenmannia EOD (see Methods).…”

Modeling the variability of the electromotor command system of pulse electric fish

“…Computational models has been previously used to answer different questions in the 265 study of electroreception and electrogenesis. Regarding electrogenesis, authors 266 in[23,26,30] used an anatomically detailed model of the pacemaker of Apteronotus 267 leptorhynchus to study the electric organ signal and its spatiotemporal features in 268 wave-type fish. In[29] a model for the Eigenmannia was employed to address the 269 jamming avoidance response in these fish.…”

Rapid evolution of a voltage-gated sodium channel gene in a lineage of electric fish leads to a persistent sodium current

“…Some species emit electric organ signals that are biophysically extreme [ 9 , 11 – 13 ]. One family within South American electric fish, the Apteronotidae, generates the highest electric organ discharge frequencies of any electric fish (depending on species, 650–1,800 Hz) [ 14 – 16 ].…”