Ruben Budelli

Electric fish measure distance in the dark

Distance determination in animals can be achieved by visual or non-visual cues. Weakly electric fish use active electrolocation for orientation in the dark. By perceiving self-produced electric signals with epidermal electroreceptors, fish can detect, locate and analyse nearby objects. Distance discrimination, however, was thought to be hardly possible because it was assumed that confusing ambiguity could arise with objects of unknown sizes and materials. Here we show that during electrolocation electric fish can measure the distance of most objects accurately, independently of size, shape and material. Measurements of the ‘electric image’ projected onto the skin surface during electrolocation revealed only one parameter combination that was unambiguously related to object distance: the ratio between maximal image slope and maximal image amplitude. However, slope-to-amplitude ratios for spheres were always smaller than those for other objects. As predicted, these objects were erroneously judged by the fish to be further away than all other objects at an identical distance. Our results suggest a novel mechanism for depth perception that can be achieved with a single, stationary two-dimensional array of detectors.

The electric image in weakly electric fish: I. A data-based model of waveform generation in Gymnotus carapo.

Understanding how electrosensory images are generated and perceived in actively electrolocating fish requires the study of the characteristics of fish bodies as electric sources. This paper presents a model ofGymnotus carapo based on measurements of the electromotive force generated by the electric organ and the impedance of the passive tissues. A good agreement between simulated and experimentally recorded transcutaneous currents was obtained. Passive structures participate in the transformation of the electromotive force pattern into transcutaneous current profiles. These spatial filtering properties of the fishs body were investigated using the model. The shape of the transcutaneous current profiles depends on tissue resistance and on the geometry and size of the fish. Skin impedance was mainly resistive. The effect of skin resistance on the spatial filtering properties of the fishs body was theoretically analyzed.The model results show that generators in the abdominal and central regions produce most of the currents through the head. This suggests that the electric organ discharge (EOD), generated in the abdominal and central regions is critical for active electrolocation. In addition, the well-synchronized EOD components generated all along the fish produce large potentials in the far field. These components are probably involved in long-distance electrocommunication.Preliminary results of this work were published as a symposium abstract.

Electric imaging through active electrolocation: implication for the analysis of complex scenes

The electric sense of mormyrids is often regarded as an adaptation to conditions unfavourable for vision and in these fish it has become the dominant sense for active orientation and communication tasks. With this sense, fish can detect and distinguish the electrical properties of the close environment, measure distance, perceive the 3-D shape of objects and discriminate objects according to distance or size and shape, irrespective of conductivity, thus showing a degree of abstraction regarding the interpretation of sensory stimuli. The physical properties of images projected on the sensory surface by the fish’s own discharge reveal a “Mexican hat” opposing centre-surround profile. It is likely that computation of the image amplitude to slope ratio is used to measure distance, while peak width and slope give measures of shape and contrast. Modelling has been used to explore how the images of multiple objects superimpose in a complex manner. While electric images are by nature distributed, or ‘blurred” behavioural strategies orienting sensory surfaces and the neural architecture of sensory processing networks both contribute to resolving potential ambiguities. Rostral amplification is produced by current funnelling in the head and chin appendage regions, where high density electroreceptor distributions constitute foveal regions. Central magnification of electroreceptive pathways from these regions particularly favours the detection of capacitive properties intrinsic to potential living prey. Swimming movements alter the amplitude and contrast of pre-receptor object-images but image modulation is normalised by central gain-control mechanisms that maintain excitatory and inhibitory balance, removing the contrast-ambiguity introduced by self-motion in much the same way that contrast gain-control is achieved in vision.

Theoretical Analysis of Pre-Receptor Image Conditioning in Weakly Electric Fish

Electroreceptive fish detect nearby objects by processing the information contained in the pattern of electric currents through the skin. The distribution of local transepidermal voltage or current density on the sensory surface of the fishs skin is the electric image of the surrounding environment. This article reports a model study of the quantitative effect of the conductance of the internal tissues and the skin on electric image generation in Gnathonemus petersii (Günther 1862). Using realistic modelling, we calculated the electric image of a metal object on a simulated fish having different combinations of internal tissues and skin conductances. An object perturbs an electric field as if it were a distribution of electric sources. The equivalent distribution of electric sources is referred to as an objects imprimence. The high conductivity of the fish body lowers the load resistance of a given objects imprimence, increasing the electric image. It also funnels the current generated by the electric organ in such a way that the field and the imprimence of objects in the vicinity of the rostral electric fovea are enhanced. Regarding skin conductance, our results show that the actual value is in the optimal range for transcutaneous voltage modulation by nearby objects. This result suggests that “voltage” is the answer to the long-standing question as to whether current or voltage is the effective stimulus for electroreceptors. Our analysis shows that the fish body should be conceived as an object that interacts with nearby objects, conditioning the electric image. The concept of imprimence can be extended to other sensory systems, facilitating the identification of features common to different perceptual systems.

Physical basis of distance discrimination in weakly electric fish

Electrolocation is a sensory system of the weakly electric fish which are able to sense the deformation of a self-generated electric field. The discrimination of distance is achieved using clues obtained from the distortion, produced by the object, on the field through the skin. Theoretical and simulation results allow us to found the hypothesis that the maximum relative slope of the profile is a good candidate parameter for distance discrimination in electrolocation.

Fish Geometry and Electric Organ Discharge Determine Functional Organization of the Electrosensory Epithelium

Active electroreception in Gymnotus omarorum is a sensory modality that perceives the changes that nearby objects cause in a self generated electric field. The field is emitted as repetitive stereotyped pulses that stimulate skin electroreceptors. Differently from mormyriformes electric fish, gymnotiformes have an electric organ distributed along a large portion of the body, which fires sequentially. As a consequence shape and amplitude of both, the electric field generated and the image of objects, change during the electric pulse. To study how G. omarorum constructs a perceptual representation, we developed a computational model that allows the determination of the self-generated field and the electric image. We verify and use the model as a tool to explore image formation in diverse experimental circumstances. We show how the electric images of objects change in shape as a function of time and position, relative to the fishs body. We propose a theoretical framework about the organization of the different perceptive tasks made by electroreception: 1) At the head region, where the electrosensory mosaic presents an electric fovea, the field polarizing nearby objects is coherent and collimated. This favors the high resolution sampling of images of small objects and perception of electric color. Besides, the high sensitivity of the fovea allows the detection and tracking of large faraway objects in rostral regions. 2) In the trunk and tail region a multiplicity of sources illuminate different regions of the object, allowing the characterization of the shape and position of a large object. In this region, electroreceptors are of a unique type and capacitive detection should be based in the pattern of the afferents response. 3) Far from the fish, active electroreception is not possible but the collimated field is suitable to be used for electrocommunication and detection of large objects at the sides and caudally.

Subthreshold sodium current underlies essential functional specializations at primary auditory afferents

Primary auditory afferents are generally perceived as passive, timing-preserving lines of communication. Contrasting this view, identifiable auditory afferents to the goldfish Mauthner cell undergo potentiation of their mixed--electrical and chemical--synapses in response to high-frequency bursts of activity. This property likely represents a mechanism of input sensitization because they provide the Mauthner cell with essential information for the initiation of an escape response. Consistent with this synaptic specialization, we show here that these afferents exhibit an intrinsic ability to respond with bursts of 200-600 Hz and this property critically relies on the activation of a persistent sodium current, which is counterbalanced by the delayed activation of an A-type potassium current. Furthermore, the interaction between these conductances with the membrane passive properties supports the presence of electrical resonance, whose frequency preference is consistent with both the effective range of hearing in goldfish and the firing frequencies required for synaptic facilitation, an obligatory requisite for the induction of activity-dependent changes. Thus our data show that the presence of a persistent sodium current is functionally essential and allows these afferents to translate behaviorally relevant auditory signals into patterns of activity that match the requirements of their fast and highly modifiable synapses. The functional specializations of these neurons suggest that auditory afferents might be capable of more sophisticated contributions to auditory processing than has been generally recognized.

Electric Imaging through Evolution, a Modeling Study of Commonalities and Differences

Modeling the electric field and images in electric fish contributes to a better understanding of the pre-receptor conditioning of electric images. Although the boundary element method has been very successful for calculating images and fields, complex electric organ discharges pose a challenge for active electroreception modeling. We have previously developed a direct method for calculating electric images which takes into account the structure and physiology of the electric organ as well as the geometry and resistivity of fish tissues. The present article reports a general application of our simulator for studying electric images in electric fish with heterogeneous, extended electric organs. We studied three species of Gymnotiformes, including both wave-type (Apteronotus albifrons) and pulse-type (Gymnotus obscurus and Gymnotus coropinae) fish, with electric organs of different complexity. The results are compared with the African (Gnathonemus petersii) and American (Gymnotus omarorum) electric fish studied previously. We address the following issues: 1) how to calculate equivalent source distributions based on experimental measurements, 2) how the complexity of the electric organ discharge determines the features of the electric field and 3) how the basal field determines the characteristics of electric images. Our findings allow us to generalize the hypothesis (previously posed for G. omarorum) in which the perioral region and the rest of the body play different sensory roles. While the “electrosensory fovea” appears suitable for exploring objects in detail, the rest of the body is likened to a “peripheral retina” for detecting the presence and movement of surrounding objects. We discuss the commonalities and differences between species. Compared to African species, American electric fish show a weaker field. This feature, derived from the complexity of distributed electric organs, may endow Gymnotiformes with the ability to emit site-specific signals to be detected in the short range by a conspecific and the possibility to evolve predator avoidance strategies.

Two-neuron networks

The behavior of two pacemaker neurons simulated by leaky integrators and connected reciprocally by synapses was studied. In every case the firing of both neurons phase-locks. The resulting limit cycle may or may not show simultaneous firing of both neurons. When both synapses are excitatory, phase-locking with simultaneous neuronal firing is always present. When one synapse is excitatory and the other inhibitory, phase-locking is also present always, while the neurons may or may not fire simultaneously. For a restricted set of parameters, bistability appears; the initial conditions determine whether or not the limit cycle presents simultaneous firing. When both synapses are inhibitory, the system phase-locks without simultaneous firing for almost every set of parameters.

Mind the gap: the minimal detectable separation distance between two objects during active electrolocation

In a food-rewarded two-alternative forced-choice procedure, it was determined how well the weakly electric elephantnose fish Gnathonemus petersii can sense gaps between two objects, some of which were placed in front of complex backgrounds. The results show that at close distances, G. petersii is able to detect gaps between two small metal cubes (2 cm × 2 cm × 2 cm) down to a width of c. 1·5 mm. When larger objects (3 cm × 3 cm × 3 cm) were used, gaps with a width of 2-3 mm could still be detected. Discrimination performance was better (c. 1 mm gap size) when the objects were placed in front of a moving background consisting of plastic stripes or plant leaves, indicating that movement in the environment plays an important role for object identification. In addition, the smallest gap size that could be detected at increasing distances was determined. A linear relationship between object distance and gap size existed. Minimal detectable gap sizes increased from c. 1·5 mm at a distance of 1 cm, to 20 mm at a distance of 7 cm. Measurements and simulations of the electric stimuli occurring during gap detection revealed that the electric images of two close objects influence each other and superimpose. A large gap of 20 mm between two objects induced two clearly separated peaks in the electric image, while a 2 mm gap caused just a slight indentation in the image. Therefore, the fusion of electric images limits spatial resolution during active electrolocation. Relative movements either between the fish and the objects or between object and background might improve spatial resolution by accentuating the fine details of the electric images.