Electric Fish:

a model system of sensory processing

Who they are: A variety of weakly electric fish exist; they come either from Africa or from South America (see geographical distribution here). The species I study most intensively is Apteronotus leptorhynchus ("Aptero" for short) and lives in the amazon river. It is nocturnal and lives in muddy waters, therefore its eyes are not very useful, instead it relies on its electrosense to navigate find preys and communicate. It is a rather shy fish and loves to hide. In the lab it hides in non-conductive plastic tubes.

Electro-sense: Weakly electric fish posses a special organ in their tail that generates electric field. In the case of Apteronotus, the field is a continuous AC current (called EOD: electric organ discharge) but some species produce discrete pulses at varying rates. Can you believe that the neurons controlling this EOD discharge fire at around 800 Hz (the EOD frequency) during the whole life of the fish! The fish has receptors on its skin allowing it to perceive the electric field and thus any distortion caused by the environment. Similarly to echolocation in bats, this is called an active sense because the animal generates the substrate that is senses. When passing by a prey (such as a Daphnia) the electric field is distorted and creates an "electrical shadow" on the skin. In fact, any object in the environment that is more -or less- conductive than the water will cause an electrical image on the electro-receptors-filled skin of the fish. Electric fishes also use their electric field to communicate with one another. Each fish has a specific EOD frequency like we all have different tone of voice. When two fish encounter, their difference in EOD frequency causes an amplitude modulation in their combined fields (called the "beat frequency"). Musician will understand the analogy with tuning of a guitar or piano: if two cord are not tuned, striking them at the same time will cause a "WooWooWoo" modulation, an amplitude beat. This beat frequency underlies the social communication of these fish. In addition males (and also sometimes females) transiently increase the frequency of their EOD (for 10 ms to ~100 ms), this is called a chirp. Chirps are an active communication effort, it can be produced in aggressive encounters (i.e. between two males) or during courtship. Note that the electric field of another Efish will affect the electroreceptors everywhere on the skin of the fish whereas preys or objects in the environment will stimulate only a small portion of the skin. The beautiful picture (figure on the right; from Krahe & Gabbiani, Nat Neurosci 2004) illustrates the electric field of fishes during communication and prey detection.

Behavior: As explained above the electric signals generated by the fish are also used to communicate. Depending on the species, electric fish can stand in large groups of a dozen (or few dozens) individuals like the glass knife fish, be surrounded by only a few individuals of the same species (e.g. the brown ghost) or more solitary like some Gymnotus species. In Apteronotus the breeding seasons is triggered by the environmental cues associated with the rainy season: decreased conductivity of water and drops falling on the water surface. Courtship behavior is hard to observe, in part because the rainy season on the Amazon has its share of dangers. Nevertheless some field studies revealed the role of courtship chirps produced by the male to attract the female. Males often engage in agonistic interactions. A simple fake electric sine wave with a frequency adequate to simulate another male is sufficient to trigger aggressive reaction in many male, especially the big ones. A fight and its outcome can serve to establish dominance of one male over another. This hierarchy is maintained within a group and translate for example in the choice of hiding place, the best ones being occupied by the alpha males. A behavior that fascinates me from the sensory point of view is the chases that they sometime engage in. Specifically, I observed in many occasions groups of Apteronotus "hanging out" together on one side of the tank (long after they were introduced in the tank, so this is not due to stress). If you observe long enough, inevitably you will witness one of them chasing another over some distance. This high speed chase must be accompanied by a roller-coaster of sensory images of the surroundings, with the EOD of several other fishes passing by, objects passing by, and in that cluttered environment the fish relies only on it electric sense, not only to navigate among tightly packed objects and conspecific, but also to lock on to the fish it is following. Several other kind of behaviors of the electric fish are being studied, in particular behaviors related to movement, navigation and spatial memory.

Electrosensory neurons: Electric Fish has elecroreceptors all over their skin. These electroreceptors project to the ELL: the electrosensory lateral line lobe. The nerve holding the electroreceptor neurons is derived from the XIIIth nerve (the one carrying auditory information in mammals). In the ELL several interneurons connect to the pyramidal cells which project to higher centers; the electrosensory information goes from there to the Torus Semicircularis, the Nucleus Electrosensorius and come back down through the motor pathway. In the ELL, a major source of inputs to pyramidal cells comes from feedback pathways through the PD and the EGP (diagram on the left). We have a thorough understanding of the connections and the molecular machinery of ELL pyramidal cells. The ELL hold three different topographic maps of its environment. The differences in channel composition and input structure leads to specialization of the different maps, Furthermore, each map contains pyramidal cells spread across different layers; these neurons also have different morphology and intrinsic dynamic. The resulting heterogeneity of pyramidal cells in the ELL underlies the sparsification of sensory processing.

Neural coding in the ELL: The ELL has been the focus of many studies of neural coding. It is also currently the focus of my research. In this short paragraph I want to summarize an important property of the pyramidal neurons of the ELL: bursting. These pyramidal cells receive feedforward inputs from their basil dendrites (from electroreceptors). Their massive apical dendrites receive feedback inputs. The morphology of these cells, with extended apical dendrites, has a huge influence on their response properties. The reason is that the apical dendrites contain active conductances that allow any action potential triggered in the soma to activate -in the apical dendrites- currents allowing the action potential to travel in these dendrites and back-propagate to the soma (see diagram on the left-hand side; from Krahe and Gabbiani, Nat Neurosci 2004). This back-propagation causes a depolarizing potential after each spike (called a DAP). This DAP increases the probability of triggering a spike shortly after each spike. Because of the increase probability of firing spikes in rapid succession the neuron produces spike in a "bursting" pattern. Bursting is a common property of neuron. One has to command the remarkable modelling effort that resulted in a so-called ghost-bursting model (so-called due to the presence of the ghost of a saddle-node bifurcation in the model). The bursting tendency is a recurrent theme in the study of these neurons (see below).

Processing of communication signals: Communication signals in the electric fish can be classified in two broad categories: involuntary signals caused by the combination of two fishes’ electric field (called “the beat”) and voluntary signals. Beat signals will not be discussed here, and remembers that any communication signals always occur on a background beat. Several types of voluntary communication signals are observed in electric fish: small and big chirps, frequency rises, interruptions... In most species, chirps are by far the most common and come in two flavours: small chirps and big chirps (figure on the left; from: Bastian et al, JEB 2001). Receptors encode these chirps with an increase in synchrony among the population or a decrease (for small and big chirps respectively). Pyramidal cells of the ELL converts this synchrony code into a detection signal encoded with bursts or a linear descriptive code for small/big chirps respectively. The next level in the nervous system, the Taurus is currently being investigated and seems to contain a variety of chirp detectors.

Here are a few lectures about the electric fish (Online resource from the Neural System & Behavior summer course at the Marine Biological Laboratory:

> A general introduction to these fish (by Eric Fortune): link here.

> A lecture about the processing of communication signals in these fish (by Gary Marsat): link here

> Sensory coding and movement (by Eric Fortune): link here

> General introduction to electroreception (by Michael Metzen): link here

This video show the response of a neuron to a "beat" stimulus as we record from it during an electrophysiological recording in awake fish.