Mormyrid fish as models for investigating sensory-motor integration: A behavioural perspective.

Animals possess senses which gather information from their environment. They can tune into important aspects of this information and decide on the most appropriate response, requiring coordination of their sensory and motor systems. This interaction is bidirectional. Animals can actively shape their perception with self-driven motion, altering sensory flow to maximise the environmental information they are able to extract. Mormyrid fish are excellent candidates for studying sensory-motor interactions, because they possess a unique sensory system (the active electric sense) and exhibit notable behaviours that seem to be associated with electrosensing. This review will take a behavioural approach to unpicking this relationship, using active electrolocation as an example where body movements and sensing capabilities are highly related and can be assessed in tandem. Active electrolocation is the process where individuals will generate and detect low-voltage electric fields to locate and recognise nearby objects. We will focus on research in the mormyrid Gnathonemus petersii (G. petersii), given the extensive study of this species, particularly its object recognition abilities. By studying object detection and recognition, we can assess the potential benefits of self-driven movements to enhance selection of biologically relevant information. Finally, these findings are highly relevant to understanding the involvement of movement in shaping the sensory experience of animals that use other sensory modalities. Understanding the overlap between sensory and motor systems will give insight into how different species have become adapted to their environments.

Electrocommunication behaviour during social interactions in two species of pulse-type weakly electric fishes (Mormyridae).

This study compares electrocommunication behaviour in groups of freely swimming weakly electric fishes of two species, Marcusenius altisambesi and Mormyrus rume. Animals emitted variable temporal sequences of stereotyped electric organ discharges (EOD) that served as communication signals. While the waveform of individual signals remained constant, the inter-discharge interval (IDI) patterns conveyed situation-specific information. Both species showed different types of group behaviour, e.g. they engaged in collective (group) foraging. The results show that in each species, during different behavioural conditions (resting, foraging and agonistic encounters), certain situation-specific IDI patterns occurred. In both species, neighbouring fishes swimming closely together interacted electrically by going in and out of synchronization episodes, i.e. periods of temporally correlated EOD production. These often resulted in echo responses between neighbours. During group foraging, fishes often signalled in a repetitive fixed order (fixed-order signalling). During foraging, EOD emission rates of M. altisambesi were higher and more regular than those of M. rume. The two species also differed in the quantity of group behaviours with M. altisambesi being more social than M. rume, which was reflected in the lack of specific agonistic IDI patterns, more fixed-order signalling and more communal resting behaviour in M. altisambesi.

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.

Coding of stimuli by ampullary afferents in Gnathonemus petersii.

Weakly electric fish use electroreception for both active and passive electrolocation and for electrocommunication. While both active and passive electrolocation systems are prominent in weakly electric Mormyriform fishes, knowledge of their passive electrolocation ability is still scarce. To better estimate the contribution of passive electric sensing to the orientation toward electric stimuli in weakly electric fishes, we investigated frequency tuning applying classical input-output characterization and stimulus reconstruction methods to reveal the encoding capabilities of ampullary receptor afferents. Ampullary receptor afferents were most sensitive (threshold: 40 µV/cm) at low frequencies (<10 Hz) and appear to be tuned to a mix of amplitude and slope of the input signals. The low-frequency tuning was corroborated by behavioral experiments, but behavioral thresholds were one order of magnitude higher. The integration of simultaneously recorded afferents of similar frequency-tuning resulted in strongly enhanced signal-to-noise ratios and increased mutual information rates but did not increase the range of frequencies detectable by the system. Theoretically the neuronal integration of input from receptors experiencing opposite polarities of a stimulus (left and right side of the fish) was shown to enhance encoding of such stimuli, including an increase of bandwidth. Covariance and coherence analysis showed that spiking of ampullary afferents is sufficiently explained by the spike-triggered average, i.e., receptors respond to a single linear feature of the stimulus. Our data support the notion of a division of labor of the active and passive electrosensory systems in weakly electric fishes based on frequency tuning. Future experiments will address the role of central convergence of ampullary input that we expect to lead to higher sensitivity and encoding power of the system.

The electric organ discharges of the Petrocephalus species (Teleostei: Mormyridae) of the Upper Volta system.

In this study, a first comparative investigation of all four species of Petrocephalus (P. bovei, P. bane, P. soudanensis and P. cf. pallidomaculatus) present in the Upper Volta system and their electric organ discharges (EOD) was conducted. It was found that P. bovei was the most widespread (in terms of habitat use), but in several places P. bovei, P. soudanensis and P. cf. pallidomaculatus occurred syntopically. All species emitted a triphasic signal, and with very few exceptions, the Petrocephalus species of the Upper Volta system could clearly be identified on the basis of their EOD waveforms. The most obvious differences between species in EOD waveforms were in amplitude of the last phase, total duration and fast Fourier transformation (FFT) peak frequency. No sexual dimorphism was present in the EOD of any species although external dimorphism, i.e. an indentation at the base of the anal fin of mature males, was common. The EOD waveform diversity in the Upper Volta principally resembled that found in four sympatric Petrocephalus species from the Ogooué system (Gabon) and might play a role in species recognition and speciation processes.

Active sensing: Pre-receptor mechanisms and behavior in electric fish.

Weakly electric fish perceive their actively generated electrical field with cutaneous electroreceptors. This active sensory system is used both for orientation and for communication. In a recent paper1 we focussed on how anatomical adaptations (pre-receptor mechanisms), biophysical constraints and behavior all contribute to active electrolocation, i.e., the fishes' unique ability to determine and distinguish the electrical properties of objects based on the modulation of a self-generated carrier signal, the so-called electric organ discharge.

Non-visual environmental imaging and object detection through active electrolocation in weakly electric fish.

Weakly electric fish orient at night by employing active electrolocation. South American and African species emit electric signals and perceive the consequences of these emissions with epidermal electroreceptors. Objects are detected by analyzing the electric images which they project onto the animal's electroreceptive skin surface. Electric images depend on size, distance, shape, and material of objects and on the morphology of the electric organ and the fish's body. It is proposed that the mormyrid Gnathonemus petersii possesses two electroreceptive "foveae" at its Schnauzenorgan and its nasal region, both of which resemble the visual fovea in the retina of many animals in design, function, and behavioral use. Behavioral experiments have shown that G. petersii can determine the resistive and capacitive components of an object's complex impedance in order to identify prey items during foraging. In addition, fish can measure the distance and three-dimensional shape of objects. In order to determine object properties during active electrolocation, the fish have to determine at least four parameters of the local signal within an object's electric image: peak amplitude, maximal slope, image width, and waveform distortions. A crucial parameter is the object distance, which is essential for unambiguous evaluation of object properties.

Nature as a model for technical sensors.

Nature has developed a stunning diversity of sensory systems. Humans and many animals mainly rely on visual information. In addition, they may use acoustic, olfactory, and tactile cues for object detection and spatial orientation. Beyond these sensory systems a large variety of highly specialized sensors have evolved. For instance, some buprestid beetles use infrared organs for the detection of forest fires. The infrared sensors of boid and crotalid snakes are used for prey detection at night. For object detection and spatial orientation many species of nocturnal fish employ active electrolocation. This review describes certain aspects of the detection and processing of infrared and electrosensory information. We show that the study of natural exotic sensory systems can lead to discoveries that are useful for the construction of technical sensors and artificial control systems. Comparative studies of animal sensory systems have the power to uncover at least a small fraction of the gigantic untapped reservoir of natural solutions for perceptive problems.

Three-dimensional analysis of object properties during active electrolocation in mormyrid weakly electric fishes (Gnathonemus petersii).

Weakly electric fishes are nocturnal and orientate in the absence of vision by using their electrical sense. This enables them not only to navigate but also to perceive and recognize objects in complete darkness. They create an electric field around their bodies by producing electric signals with specialized electric organs. Objects within this field alter the electric current at electroreceptor organs, which are distributed over almost the entire body surface. During active electrolocation, fishes detect, localize and analyse objects by monitoring their self-produced electric signals. We investigated the ability of the mormyrid Gnathonemus petersii to perceive objects three-dimensionally in space. Within a range of about 12 cm, G. petersii can perceive the distance of objects. Depth perception is independent of object size, shape and material. The mechanism for distance determination through electrolocation involves calculating the ratio between two parameters (maximal slope and maximal amplitude) of the electrical image which each object projects onto the fish's skin. During active electrolocation, electric fishes cannot only locate objects in space but in addition can determine the three-dimensional shape of an object. Up to certain limits, objects are spontaneously categorized according to their shapes, but not according to their sizes or the materials of which they are made.

The midbrain precommand nucleus of the mormyrid electromotor network.

The functional role of the midbrain precommand nucleus (PCN) of the electromotor system was explored in the weakly electric mormyrid fish Gnathonemus petersii, using extracellular recording of field potentials, single unit activity, and microstimulation in vivo. Electromotor-related field potentials in PCN are linked in a one-to-one manner and with a fixed time relationship to the electric organ discharge (EOD) command cycle, but occur later than EOD command activity in the medulla. It is suggested that PCN electromotor-related field potentials arise from two sources: (1) antidromically, by backpropagation across electrotonic synapses between PCN axons and command nucleus neurons, and (2) as corollary discharge-driven feedback arriving from the command nucleus indirectly, via multisynaptic pathways. PCN neurons can be activated by electrosensory input, but this does not necessarily activate the whole motor command chain. Microstimulation of PCN modulates the endogenous pattern of electromotor command in a way that can mimic the structure of certain stereotyped behavioral patterns. PCN activity is regulated, and to a certain extent synchronized, by corollary discharge feedback inhibition. However, PCN does not generally function as a synchronized pacemaker driving the electromotor command chain. We propose that PCN neurons integrate information of various origins and individually relay this to the command nucleus in the medulla. Some may also have intrinsic, although normally nonsynchronized, pacemaker properties. This descending activity, integrated in the electromotor command nucleus, will play an important modulatory role in the central pattern generator decision process.

Distance discrimination during active electrolocation in the weakly electric fish Gnathonemus petersii.

Weakly electric fish use active electrolocation for orientation at night. They emit electric signals (electric organ discharges) which generate an electrical field around their body. By sensing field distortions, fish can detect objects and analyze their properties. It is unclear, however, how accurately they can determine the distance of unknown objects. Four Gnathonemus petersii were trained in two-alternative forced-choice procedures to discriminate between two objects differing in their distances to a gate. The fish learned to pass through the gate behind which the corresponding object was farther away. Distance discrimination thresholds for different types of objects were determined. Locomotor and electromotor activity during distance measurement were monitored. Our results revealed that all individuals quickly learned to measure object distance irrespective of size, shape or electrical conductivity of the object material. However, the distances of hollow, water-filled cubes and spheres were consistently misjudged in comparison with solid or more angular objects, being perceived as farther away than they really were. As training continued, fish learned to compensate for these 'electrosensory illusions' and erroneous choices disappeared with time. Distance discrimination thresholds depended on object size and overall object distance. During distance measurement, the fish produced a fast regular rhythm of EOD discharges. A mechanisms for distance determination during active electrolocation is proposed.

Electroreceptor model of weakly electric fish Gnathonemus petersii: II. Cellular origin of inverse waveform tuning.

In part I (. Biophys. J. 75:1712-1726), we presented a cellular model of the A- and B-electroreceptors of the weakly electric fish Gnathonemus petersii. The model made clear the cellular origin of the differences in the response functions of A- and B-receptors, which sensitively code the intensity of the fish's own electric organ discharge (EOD) and the variations in the EOD waveform, respectively. The main purpose of the present paper is to clarify the cellular origin of the inverse waveform tuning of the B-receptors by using the receptor model. Inverse waveform tuning means that B-receptors respond more sensitively to the 180 degrees inverted EOD than to undistorted or less distorted EODs. We investigated how the A- and B-receptor models respond to EODs with various waveforms, which are the phase-shifted EODs, whose shift angle is varied from -1 degrees to -180 degrees, and single-period sine wave stimuli of various frequencies. We show that the tuning properties of the B-receptors arise mainly from the combination of two attributes: 1) The waveform of the stimuli (Bstim) effectively sensed by the B-receptor cells. This consists of a first smaller and a second larger positive peak, even though in the original phase-shifted EOD stimuli, the amplitudes of the two positive peaks are reversed. 2) The effective time constant of dynamical response of the receptor cells. It is on the order of the duration of a single EOD pulse. We also calculated the response properties of the A- and B-receptor models when stimulated with natural EODs distorted by various capacitive and resistive objects. Furthermore, we investigated the effect of EOD amplitude on the receptor responses to capacitive and resistive objects. The models presented can systematically reproduce the experimentally observed response properties of natural A- and B-receptor cells. The mechanism producing these properties can be reasonably explained by the variation in the stimulus waveforms effectively sensed by the A- and B-receptor cells and by time constants.

Orientation in the dark: brain circuits involved in the perception of electric signals in mormyrid electric fish.

Weakly electric fish produce electric signals with a specialised organ in their tail. In addition, they are electrosensitive and can perceive their self-generated signals (for electrolocation) and electric signals of other electric fishes (for electrocommunication). Mormyrids possess three types of peripheral electroreceptor organs, one used for electrocommunication and two types involved in electolocation. They are innervated by afferent fibres, which project to different zones in the electrosensory lateral line lobe (ELL) in the medulla. Brain circuits for electrolocation and electrocommunication are separated almost throughout the whole brain. Electrolocation pathways run from the ELL-cortex to the torus semicircularis of the midbrain and then via the valvula cerebelli towards the telencephalon. Pathways involved in electrocommunication run from the nucleus of the ELL to another part of the torus and from there through the isthmic granule nucleus to the valvula. In addition, a pathway via the preglomerular complex to the telencephalon might exist. In both the electrolocation and the electrocommunication circuits, prominent recurrent pathways are present.

Active electrolocation of objects in weakly electric fish

Weakly electric fish produce electric signals (electric organ discharges, EODs) with a specialised electric organ creating an electric field around their body. Objects within this field alter the EOD-induced current at epidermal electroreceptor organs, which are distributed over almost the entire body surface. The detection, localisation and analysis of objects performed by monitoring self-produced electric signals is called active electrolocation. Electric fish employ active electrolocation to detect objects that are less than 12 cm away and have electric properties that are different from those of the surrounding water. Within this range, the mormyrid Gnathonemus petersii can also perceive the distance of objects. Depth perception is independent of object parameters such as size, shape and material. The mechanism for distance determination through electrolocation involves calculating the ratio between two parameters of the electric image that the object projects onto the fish's skin. Electric fish can not only locate objects but can also analyse their electrical properties. Fish are informed about object impedance by measuring local amplitude changes at their receptor organs evoked by an object. In addition, all electric fish studied so far can independently determine the capacitative and resistive components of objects that possess complex impedances. This ability allows the fish to discriminate between living and non-living matter, because capacitance is a property of living organisms. African mormyrids and South American gymnotiforms use different mechanisms for capacitance detection. Mormyrids detect capacitance-evoked EOD waveform distortions, whereas gymnotiforms perform time measurements. Gymnotiforms measure the temporal phase shift of their EODs induced at body parts close to the object relative to unaffected body parts further away.

Neural command of electromotor output in mormyrids

The electric discharge of mormyrid fish has an irregular pattern controlled by the electromotor command nucleus in the medulla. Anatomical studies suggest that much of the descending information integrated by the command nucleus comes from the diencephalic precommand nucleus. But field potentials related to the motor command occur later in the precommand nucleus than in the command nucleus, suggesting that they are a corollary rather than a cause of electromotor command initiation. Recorded extracellularly, certain precommand nucleus units fire spontaneously between electromotor commands but pause briefly following each command; others units fire a burst of spikes only during the post-command pause. The firing frequency of the former is correlated with the duration of the interval between successive electromotor commands when the fish is discharging at more than approximately 5 Hz. The post-command pause in spontaneous firing is due to corollary-discharge-mediated feedback inhibition, probably generated by the activity of the bursting units that fire only during this period. Precommand nucleus neurons are activated by electrosensory input, and stimulation of the precommand nucleus modulates the endogenous pattern of electromotor command. We propose that the irregular rhythm of the motor command depends largely on the integration of descending information of various origins, conveyed via the precommand nucleus to the command nucleus, and that this process is regulated by corollary discharge feedback inhibition to the precommand nucleus.

Anatomical connections of auditory and lateral line areas of the dorsal telencephalon (Dm) in the osteoglossomorph teleost, Gnathonemus petersii.

Local field potentials evoked either by auditory or by mechanosensory (water displacement) lateral line stimuli were recorded in sensory subregions of the telencephalic nucleus dorsalis pars medialis (Dm) in the weakly electric fish Gnathonemus petersii. The neural tracer Neurobiotin was injected into these two physiologically defined subregions. A reciprocal connection between the two subregions of Dm, as well as cell bodies and terminals in other telencephalic regions, whose distribution was somewhat different for the two injection types, were found. The course of labeled fibers outside the telencephalon was similar after injections in both Dm regions. Fibers were seen running through the lateral forebrain bundle (lfb) to the ventral surface area of the brain within the diencephalic preglomerular region (PGv). Within a narrow streak along the ventral side of the brain densely arranged cell bodies were labeled. The locations of labeled cells within PGv were indistinguishable after tracer was injected into either acoustical or lateral line areas of Dm. Only after injection into the mechanosensory Dm region labeled cell bodies were found in the anterior preglomerular nucleus (PGa), in addition. When crystals of the fluorescent tracer DiI were inserted in the ventral part of PGv, a path of labeled fibers similar to that after telencephalic injections was found. Labeled terminals, but no cell bodies, were located both in the acoustical and in the mechanosensory regions of Dm as well as in several other telencephalic areas. Even though sensory regions in Dm that process acoustical and mechanical stimuli are segregated and unimodal, they both receive input from neurons of PGv. The specificity of the mechanosensory region of Dm might originate from the additional input from PGa and from other endbrain areas.

The "novelty response" in an electric fish: response properties and habituation.

The electromotor behavior evoked by novel sensory stimuli in the electrogenic teleost fish Gnathonemus petersii was examined. Novelty responses (NRs) consisted of a transient accelerations of the rate of electric organ discharges following a change in sensory input. NRs were basically similar in nontreated and in immobilized (treated with curare) fish. NRs could be evoked reliably by brief novel stimuli of all four sensory modalities (acoustic, visual, electrical. electrolocation) used in this study. Stimuli of a duration longer than 5 s caused an on- and off-response. A sudden change in the quality of an ongoing sensory stimulus also evoked novelty responses. NR properties depended on the stimulus modality, stimulus intensity, stimulus duration, and on the prior stimulus history. Habituation of several response parameters of the NR (latency, duration, maximal amplitude, response probability) occurred within a series of repetitive stimuli of a given sensory modality. Each modality appeared to habituate separately. Rate of habituation depended on stimulus intensity and on interstimulus interval. A strong disruptive stimulus of another modality lead to dishabituation. The novelty response evoked by stimuli of low or medium intensities resembled an "orienting response" as described by Sokolov.

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.

Sensory processing in the pallium of a mormyrid fish.

To investigate the functional organization of higher brain levels in fish we test the hypothesis that the dorsal gray mantle of the telencephalon of a mormyrid fish has discrete receptive areas for several sensory modalities. Multiunit and compound field potentials evoked by auditory, visual, electrosensory, and water displacement stimuli in this weakly electric fish are recorded with multiple semimicroelectrodes placed in many tracks and depths in or near telencephalic area dorsalis pars medialis (Dm). Most responsive loci are unimodal; some respond to two or more modalities. Each modality dominates a circumscribed area, chiefly separate. Auditory and electrical responses cluster in the dorsal 500 micrometer of rostral and caudolateral Dm, respectively. Two auditory subdivisions underline specialization of this sense. Mechanoreception occupies a caudal area overlapping electroreception but centered 500 micrometer deeper. Visual responses scatter widely through ventral areas. Auditory, electrosensory, and mechanosensory responses are dominated by a negative wave within the first 50 msec, followed by 15-55 Hz oscillations and a slow positive wave with multiunit spikes lasting from 200 to 500 msec. Stimuli can induce shifts in coherence of certain frequency bands between neighboring loci. Every electric organ discharge command is followed within 3 msec by a large, mainly negative but generally biphasic, widespread corollary discharge. At certain loci large, slow ("deltaF") waves usually precede transient shifts in electric organ discharge rate. Sensory-evoked potentials in this fish pallium may be more segregated than in elasmobranchs and anurans and have some surprising similarities to those in mammals.

Finding food: senses involved in foraging for insect larvae in the electric fish gnathonemus petersii

The weakly electric fish Gnathonemus petersii searches at night for insect larvae in tropical African streams. The aim of this study was to determine the contributions of different sensory modalities to foraging. The time that fish needed to find two randomly placed chironomid larvae was measured. The influence of various senses on search time was investigated by blocking the use of one or more senses. Active electrolocation was used by most fish for prey detection in the dark. In addition, passive electrolocation played a role in some individuals. If light was available, vision could become the dominant sense in some individuals, replacing active electrolocation. The presence of chemical cues decreased prey detection time in most fish. Prey movements also shortened search times when active electrolocation and vision were not possible, indicating that the mechanosensory lateral line also plays a role in the detection of moving prey. The results show that G. petersii uses several senses simultaneously during foraging. Each individual favours a specific combination of the available sensory inputs. If one sensory modality is eliminated, fish can switch to other modalities, indicating that the food detection system is flexible and plastic.