This review addresses the biophysical mechanisms of image formation in electrosensory systems. These electrical images are used for navigation and object detection by many species of fish, some amphibians, and some mammals. In the active electrosensory systems of fish these images are formed by the fish's own electric organ discharge. In the passive electrosensory systems of fish, amphibians and mammals the images are formed by external electrical sources. In this review we describe the biophysics of image formation, the effects of the organism's passive electrical properties, the role of exploration, and the influence of context on electroreception. We suggest that the basic principles established in these specialized systems be useful for understanding other more common sensory systems.
Understanding fixed motor pattern diversity across related species provides a window for exploring the evolution of their underlying neural mechanisms. The electric organ discharges of weakly electric fishes offer several advantages as paradigmatic models for investigating how a neural decision is transformed into a spatiotemporal pattern of action. Here, we compared the far fields, the near fields and the electromotive force patterns generated by three species of the pulse generating New World gymnotiform genus Gymnotus. We found a common pattern in electromotive force, with the far field and near field diversity determined by variations in amplitude, duration, and the degree of synchronization of the different components of the electric organ discharges. While the rostral regions of the three species generate similar profiles of electromotive force and local fields, most of the species-specific differences are generated in the main body and tail regions of the fish. This causes that the waveform of the field is highly site dependant in all the studied species. These findings support a hypothesis of the relative separation of the electrolocation and communication carriers. The presence of early head negative waves in the rostral region, a species-dependent early positive wave at the caudal region, and the different relationship between the late negative peak and the main positive peak suggest three points of lability in the evolution of the electrogenic system: a) the variously timed neuronal inputs to different groups of electrocytes; b) the appearance of both rostrally and caudally innervated electrocytes, and c) changes in the responsiveness of the electrocyte membrane.
This article reports some contextual effects of fish hovering in small environments on active imaging. Foveal electrosensory images of objects and their corresponding evoked responses in the electrosensory lobe are altered in amplitude and waveform when the fish are inside tubes. The article describes: (i) the physical basis of the changes imposed by small environments on electric images, (ii) the field potential responses at the electrosensory lobe of chronically implanted animals when entering and leaving tubes, and (iii) the effect of context on object discrimination. Biophysical analysis indicates that tubes cause a change in the efficiency of a previously described pre-receptor/post-effector mechanism responsible for the electric 'illumination' of nearby objects (as mirrors change the illumination of visual scenes). Field potential responses at the electrosensory lobe showed two components corresponding to the fast-and slowelectrosensory pathways respectively: (a) an early spike following the input without adaptation; (b) a series of waves lasting the rest of the cycle and exhibiting different degrees of adaptation. Discrimination experiments showed that fish react to changes in image rather than to changes in object resistance. The amplitude of the novelty responses evoked by similar changes in the total energy of electric images was constant despite the large change in basal stimulus amplitude and waveform caused by hovering in the tubes. These facts may be explained by the presence of adaptive responses observed at the slow pathway in the electrosensory lobe.
SUMMARYThis article reports a biophysical and behavioral assessment of the active electrolocation range of Gymnotus omarorum. Physical measurements show that the stimulus field of a point on the sensory mosaic (i.e. the potential positions in which an object may cause a significant departure of the transcutaneous field from basal in the absence of an object) consists of relatively extended volumes surrounding this point. The shape of this stimulus field is dependent on the position of the point on the receptive mosaic and the size of the object. Although the limit of stimulus fields is difficult to assess (it depends on receptor threshold), departure from the basal field decays rapidly, vanishing at about 1.5 diameters for conductive spheres. This short range was predictable from earlier theoretical constructs and experimental data. Here, we addressed the contribution of three different but synergetic mechanisms by which electrosensory signals attenuate with object distance. Using novelty responses as an indicator of object detection we confirmed that the active electrosensory detection range is very short. Behavioral data also indicate that the ability to precisely locate a small object of edible size decays even more rapidly than the ability to detect it. The role of active electroreception is discussed in the context of the fishʼs habitat.
This article deals with the role of fish's body and object's geometry on determining the image spatial shape in pulse Gymnotiforms. This problem was explored by measuring local electric fields along a line on the skin in the presence and absence of objects. We depicted object's electric images at different regions of the electrosensory mosaic, paying particular attention to the perioral region where a fovea has been described. When sensory surface curvature increases relative to the object's curvature, the image details depending on object's shape are blurred and finally disappear. The remaining effect of the object on the stimulus profile depends on the strength of its global polarization. This depends on the length of the object's axis aligned with the field, in turn depending on fish body geometry. Thus, fish's body and self-generated electric field geometries are embodied in this “global effect” of the object. The presence of edges or local changes in impedance at the nearest surface of closely located objects adds peaks to the image profiles (“local effect” or “object's electric texture”). It is concluded that two cues for object recognition may be used by active electroreceptive animals: global effects (informing on object's dimension along the field lines, conductance, and position) and local effects (informing on object's surface). Since the field has fish's centered coordinates, and electrosensory fovea is used for exploration of surfaces, fish fine movements are essential to perform electric perception. We conclude that fish may explore adjacent objects combining active movements and electrogenesis to represent them using electrosensory information.
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