Learning Neurobiology with electric fish

Electric Gymnotiform fish live in muddy, shallow waters near the shore – hiding in the dense filamentous roots of floating plants such as Eichornia crassipes (“camalote”). They explore their surroundings by using a series of electric pulses that serve as self emitted carrier of electrosensory signals. This propagates at the speed of light through this spongiform habitat and is barely sensed by the lateral line of predators and prey. The emitted field polarizes the surroundings according to the difference in impedance with water which in turn modifies the profile of transcutaneous currents considered as an electrosensory image. Using this system, pulse Gymnotiformes create an electrosensory bubble where an object’s location, impedance, size and other characteristics are discriminated and probably recognized. Although consciousness is still not well-proven, cognitive functions as volition, attention, and path integration have been shown. Here I will summarize different aspects of the electromotor electrosensory loop of pulse Gymnotiforms. First, I will address how objects are polarized with a stereotyped but temporospatially complex electric field, consisting of brief pulses emitted at regular intervals. This relies on complex electric organs quasi periodically activated through an electromotor coordination system by a pacemaker in the medulla. Second, I will deal with the imaging mechanisms of pulse gymnotiform fish and the presence of two regions in the electrosensory field, a rostral region where the field time course is coherent and field vector direction is constant all along the electric organ discharge and a lateral region where the field time course is site specific and field vector direction describes a stereotyped 3D trajectory. Third, I will describe the electrosensory mosaic and their characteristics. Receptor and primary afferents correspond one to one showing subtypes optimally responding to the time course of the self generated pulse with a characteristic train of spikes. While polarized objects at the rostral region project their electric images on the perioral region where electrosensory receptor density, subtypes and central projection are maximal, the image of objects on the side recruit a single type of scattered receptors. Therefore, the rostral mosaic has been likened to an electrosensory fovea and its receptive field referred to as foveal field. The rest of the mosaic and field are referred to as peripheral. Finally, I will describe ongoing work on early processing structures. I will try to generate an integrated view, including anatomical and functional data obtained in vitro, acute experiments, and unitary recordings in freely moving fish. We have recently shown have shown that these fish tract allo-generated fields and the virtual fields generated by nearby objects in the presence of self-generated fields to explore the nearby environment. These data together with the presence of a multimodal receptor mosaic at the cutaneous surface particularly surrounding the mouth and an important role of proprioception in early sensory processing suggests the hypothesis that the active electrosensory system is part of a multimodal haptic sense.