Several animals are renowned for their cognitive skills such as tool use, metacognition or social learning. However, it remains puzzling why some species excel whereas others – sometimes even closely related ones ¬– do not. Archerfish show a remarkable assembly of skills in the context of their unique hunting behavior in which they down aerial prey with shots of water. Hoping to find ecological factors behind these skills, we have, over the past years, regularly traveled to archerfish mangrove habitats in Thailand. One of the most consistent findings was the presence of other surface-feeding fish, particularly the similar-sized halfbeak Zenarchopterus buffonis, wherever we spotted groups of archerfish. We describe here that Zenarchopterus is superbly equipped with water-wave detectors, rapidly detects the impact of prey even in the dark, is active at all times, is usually more numerous than archerfish and supplements its capabilities with visual skills. Without sophisticated additions to their hunting technique archerfish would thus lose most of their downed prey to halfbeaks. We suggest that the evolution of several skills of archerfish may have thus been influenced not only by intraspecific competition but also by competition with other surface-feeding fish.
Neuronal cell cultures offer a crucial tool to mechanistically analyse regeneration in the nervous system. Despite the increasing importance of zebrafish (Danio rerio) as an in vivo model in neurobiological and biomedical research, in vitro approaches to the nervous system are lagging far behind and no method is currently available for establishing enriched neuronal cell cultures. Here we show that magnetic-activated cell sorting (MACS) can be used for the large-scale generation of neuronal restricted progenitor (NRP) cultures from embryonic zebrafish. Our findings provide a simple and semi-automated method that is likely to boost the use of neuronal cell cultures as a tool for the mechanistic dissection of key processes in neuronal regeneration and development.
Among tool-using animals, none are known to adaptively change the hydrodynamic properties of a free jet of water—a task considered difficult in human technology. Hunting archerfish can strike their targets with precisely aimed water jets, but they are also presently thought to be unable to actively control the hydrodynamics of their jets. By using specifically trained fish, we were able to monitor several aspects of jet production and propagation as the fish fired at targets over a much wider range of distances than previously explored. We show that jets that have to travel farther also live longer. Furthermore, the time needed until water assembles at the jet tip is not fixed. Rather, it is adjusted so that maximum focusing occurs just before impact. Surprisingly, the fish achieve this by modulating the dynamics of changes in the cross-section of their mouth opening, a mechanism that seems to not have been applied yet in human-built nozzles. The timing adjustments archerfish make in order to powerfully hit targets over an extended range strikingly parallel the situation in the “uniquely human” ability of powerful throwing. Based on the key role throwing played in human encephalization and cognitive evolution, skillfully “throwing” water should similarly have led to the correlated rapid evolution of cognitive skills in this animal.
In their unique hunting behaviour, archerfish use a complex motor decision to secure their prey: based solely on how dislodged prey initially falls, they select an adapted C-start manoeuvre that turns the fish right towards the point on the water surface where their prey will later land. Furthermore, they take off at a speed that is set so as to arrive in time. We show here that the C-start manoeuvre and not subsequent tail beating is necessary and sufficient for setting this adaptive level of speed. Furthermore, the C-start pattern is adjusted to independently determine both the turning angle and the take-off speed. The selection of both aspects requires no a priori information and is done based on information sampled from the onset of target motion until the C-start is launched. Fin strokes can occur right after the C-start manoeuvre but are not required to fine-tune take-off speed, but rather to maintain it. By probing the way in which the fish set their take-off speed in a wide range of conditions in which distance from the later catching point and time until impact varied widely and unpredictably, we found that the C-start manoeuvre is programmed based on pre-C-start estimates of distance and time until impact. Our study hence provides the first evidence for a C-start that is fine-tuned to produce an adaptive speed level.
This article presents a summary and critical review of what is known about the ‘grouped retina’, a peculiar type of retinal organization in fish in which groups of photoreceptor cell inner and outer segments are arranged in spatially separated bundles.
Hunting archerfish precisely adapt their predictive C-starts to the initial movement of dislodged prey so that turn angle and initial speed are matched to the place and time of the later point of catch. The high accuracy and the known target point of the starts allow a sensitive straightforward assay of how temperature affects the underlying circuits. Furthermore, archerfish face rapid temperature fluctuations in their mangrove biotopes which could compromise performance. Here we show that after a brief acclimation period the function of the C-starts is fully maintained over a range of operating temperatures: (i) Full responsiveness was maintained at all temperatures, (ii) at all temperatures the fish selected accurate turns and were able to do so over the full angular range, (iii) at all temperatures speed attained immediately after the end of the C-start was matched - with equal accuracy - to 'virtual speed', i.e. the ratio of remaining distance to the future landing point and remaining time. While precision was fully compensated, C-start latency was not and increased by about 4 ms per 1°C cooling. Also kinematic aspects of the C-start were only partly compensated. Above 26°C the duration of the two major phases of the C-start were temperature-compensated. At lower temperatures, however, durations increased similarly as latency. Given the accessibility of the underlying networks, the archerfish predictive start should be an excellent model to assay the degree of plasticity and functional stability of C-start motor patterns.
Archerfish are renowned for shooting down aerial prey with water jets, but nothing is known about the ways they spot prey items in their richly structured mangrove habitats. We trained archerfish to stably assign the categories 'target' and 'background' to objects solely on the basis of non-motion cues. Unlike many other hunters archerfish are able to discriminate a target from its background in the complete absence of either self-motion or relative motion parallax cues and without using stored information about the structure of the background. This allowed us to perform matched tests to compare the ways fish and humans scan stationary visual scenes. In humans, visual search is seen as a doorway to cortical mechanisms of how attention is allocated. Fish lack a cortex and we therefore wondered if archerfish would differ from humans in their ways they scan a stationary visual scene. Our matched tests failed to disclose any differences in the dependence of response time distributions, a most sensitive indicator of the search mechanism, on number and complexity of background objects. Median and range of response times depended linearly on the number of background objects and the corresponding effective processing time per item increased similarly - about fourfold - in both humans and fish when the task was harder. Archerfish, like humans, also systematically scanned the scenery, starting with the closest object. Taken together, benchmark visual search tasks failed to disclose any difference between archerfish - who lack a cortex - and humans.
Decision-making networks must be tuned according to the rules that govern which action will be rewarded for a given constellation of current sensory information. Somehow these rules must be implemented in the networks that translate the sensory cues to actions but the nature of this representation is enigmatic. Recent findings suggest that Mauthner-associated networks in some fish can govern surprisingly sophisticated and plastic decisions in which the rules of prey motion govern what speed and direction must be selected to be at the right point at the right time. With the key cellular players individually identifiable, fish can help us to discover the nature of how rules are represented in decision-making circuitry of the vertebrate brain.
Despite their diversity, vertebrate retinae are specialized to maximize either photon catch or visual acuity. Here, we describe a functional type that is optimized for neither purpose. In the retina of the elephantnose fish (Gnathonemus petersii), cone photoreceptors are grouped together within reflecting, photonic crystal–lined cups acting as macroreceptors, but rod photoreceptors are positioned behind these reflectors. This unusual arrangement matches rod and cone sensitivity for detecting color-mixed stimuli, whereas the photoreceptor grouping renders the fish insensitive to spatial noise; together, this enables more reliable flight reactions in the fish’s dim and turbid habitat as compared with fish lacking this retinal specialization.
With more than 30 000 species inhabiting nearly every aquatic environment on earth, fish provide a rich source for studying fundamental aspects of visual processing. Many fish show highly sophisticated visual behaviors that often allow the analysis of unique visual specializations. Furthermore, most fish can readily be trained. This was masterly used to dismount the claim that lower vertebrates and invertebrates could not see color. Interestingly, later Nobel laureate Karl von Frisch first succeeded to show this in fish, before his famous work on bees. In this article, we will illustrate a number of behavioral approaches that have been used successfully to tackle most aspects of fish vision.
... After a brief overview of complex decisions in primates and of decision-making in simple networks, I argue that simpler systems can combine complexity with accessibility at the cellular level. Indeed, examination of a network in fish may help in dissecting key mechanisms of complex and flexible decision-making in an established model of synaptic plasticity at the level of identified neurons.
Numerous animal navigators are not simply at the mercy of winds and currents but cope with drift to reach their goals. Here, we report how a fruit-catching Costa Rican fish combines an analysis of aerial motion with a novel way of compensating for drift to optimize its catching success. In the field, schools of this riverine fish never waited until a falling fruit actually landed in the stream. Rather, the fish responded to visual motion and started early to arrive on time at the spot where their food would land. To be successful with their early starts, the fish must cope with the strong relative drift that arises, because the fish, but not their airborne target, experience strong flow on their way toward the fruit’s landing point. Surprisingly, the fish solve this problem right at the beginning—by turning rapidly and taking an initial aim that is already optimally adapted to the prevailing drift, so as to lead them straight to their food. Fruit-catching fish thus provide a stunning case of how rapidly animals can generate drift-compensating trajectories in their everyday local lives.
The enormous progress made in functional magnetic resonance imaging technology allows us to watch our brains engage in complex cognitive and social tasks. However, our understanding of what actually is computed in the underlying cellular networks is hindered by the vast numbers of neurons involved. Here, we describe a vertebrate system, shaped for top speed, in which a complex and plastic decision is performed by surprisingly small circuitry that can be studied at cellular resolution.
Once their shots have successfully dislodged aerial prey, hunting archer fish monitor the initial values of their prey’s ballistic motion and elicit an adapted rapid turning maneuver. This allows these fish to head straight towards the later point of catch with a speed matched to the distance to be covered. To make the catch despite severe competition the fish must quickly and yet precisely match their turn and take-off speed to the initial values of prey motion. However, the initial variables vary over broad ranges and can be determined only after prey is dislodged. Therefore, the underlying neuronal circuitry must be able to drive a maneuver that combines a high degree of precision and flexibility at top speed. To narrow down which neuronal substrate underlies the performance we characterized the kinematics of archer fish predictive starts using digital high-speed video. Strikingly, the predictive starts show all hallmarks of Mauthner-driven teleost C-type fast-starts, which have previously not been noted in feeding strikes and were not expected to provide the high angular accuracy required. The high demands on flexibility and precision of the predictive starts do not compromise their performance. On the contrary, archer fish predictive starts are among the fastest C-starts known so far among teleost fish, with peak linear speed beyond 20·body·lengths·s–1, angular speed over 4500·deg.·s–1, maximum linear acceleration of up to 12 times gravitational acceleration and peak angular acceleration of more than 450·000·deg.·s–2. Moreover, they were not slower than archer fish escape C-starts, elicited in the same individuals. Rather, both escapes and predictive starts follow an identical temporal pattern and all kinematic variables of the two patterns overlap. This kinematic equivalence strongly suggests that archer fish recruit their C-start escape network of identified reticulospinal neurons, or elements of it, to drive their predictive starts. How the network drives such a rather complex behavior without compromising speed is a wide open question.
... The fish appear to learn in ways that most high-school students and perhaps even more their teachers would dream of. A remarkable capability to generalize allows them to readily engage demanding tasks they have not directly been exposed to before.
A recent study has shown that, unusually, both the sensory and motor capabilities of an electric fish are omnidirectional. This matching of motor and sensory spaces helps the fish to hunt prey efciently —particularly important given their energetically costly active sensory system.
Archer fish can shoot down insect prey with a sharp jet of water. Fish usually fire from positions that are not directly below their target so that a dislodged insect falls ballistically with a horizontal velocity component. Only 100·ms after the insect is on its path both the shooter and other school members can initiate a rapid turn and then head straight in the direction of the later point of impact of their falling prey. The quick turn and subsequent take- off are performed ‘open-loop’, based on the initial values of the falling insect’s motion. We report here that archer fish can not only take off in the direction of the later point of impact but also predict its distance. Distance information allows the fish to adjust their take-off speed so that they would arrive within a narrow time slot slightly (about 50·ms) after their prey’s impact, despite large differences in the size of the aligning turn and in the distance to be covered. Selecting a constant speed program with matched speed and catching the insect on the move minimizes frictional losses. The initial speed of starting fish is slightly but systematically too slow and is increased later so that the fish arrive 20·ms earlier than expected and often make the catch on a higher than take-off speed. The variability of later speed changes suggests a systematic ‘error’ in the take-off, as if the fish underestimated distance. However, this apparent deficiency seems well adapted to the fish catching their prey at a high speed: if later the fish had no possibility to correct an initial error then it is better to start slightly too slow in order to minimize the risk of overshooting the point of catch.
Studying for the first time the forces transferred to prey, we discovered that archerfish do not fire all-or-none shots but fine-tune their surprisingly costly shots to prey size. This tuning is strikingly lacking of plasticity and innately matched to a constant key property of archerfish feeding ecology: the universal scaling of adhesive forces of their various prey organisms.
In extremely rapid maneuvers, animals including man can launch ballistic motor patterns that cannot immediately be corrected [1–3]. Such patterns are difficult to direct at targets that move in three-dimensional space [2–4], and it is presently unknown how animals learn to acquire the precision required. Archer fish live in groups and are renowned for their ballistic hunting technique in which they knock down stationary aerial insect prey with a precisely aimed shot of water [5– 7]. Here we report that these fish can learn to release their shots so as to hit prey that moves rapidly at great height, a remarkable accomplishment in which the shooter must take both the target’s three-dimensional motion as well as that of its rising shot into account. To successfully perform in the three-dimensional task, training with horizontal motion suffices. Moreover, all archer fish of a group were able to learn the complex sensomotor skill from watching a performing group member, without having to practice. This instance of social learning in a fish is most remarkable as it could imply that observers can ‘‘change their viewpoint,’’ mapping the perceived shooting characteristics of a distant team member into angles and tar- get distances that they later must use to hit.
Why study hearing and vision in electric fish whose outstanding electromotor and electrosensory abilities enable them to exchange messages 'secretly' over a channel that is inaccessible to most other animals?
Many animals, including humans, can visually judge the absolute size of objects regardless of changes in viewing distance and thus despite the resulting dramatic differences in the size of the actual retinal images [1–5]. For animals that have to judge the size of aerial objects from underwater views, this can be a formidable problem; our calculations show that considerable and strongly viewpoint-dependent corrections are needed to compensate for the effects of light refraction. Archer fish face these optical difficulties because they have to shoot down aerial insects over a wide range of horizontal and vertical distances [6, 7]. We show here that these fish can learn to acquire size constancy with remarkable precision and are thus fully capable of taking complex viewpoint dependency into account. Moreover, we demonstrate that archer fish solve the problem not by interpolating within a set of stored views and distances but by learning the laws that connect apparent size with the fish’s relative position to the target. This enables the fish to readily judge the absolute sizes of objects from completely novel views.
Insects can estimate distance or time-to-contact of surrounding objects from locomotion-induced changes in their retinal position and/or size. Freely walking fruit flies (Drosophila melanogaster) use the received mixture of different distance cues to select the nearest objects for subsequent visits. Conventional methods of behavioral analysis fail to elucidate the underlying data extraction. Here we demonstrate first comprehensive solutions of this problem by substituting virtual for real objects; a tracker-controlled 360 deg panorama converts a fruit fly’s changing coordinates into object illusions that require the perception of specific cues to appear at preselected distances up to infinity. An application reveals the following: (1) en- route sampling of retinal-image changes accounts for distance discrimination within a surprising range of at least 8–80 body lengths (20–200 mm). Stereopsis and peering are not involved. (2) Distance from image translation in the expected direction (motion parallax) outweighs distance from image expansion, which accounts for impact-avoiding flight reactions to looming objects. (3) The ability to discriminate distances is robust to artificially delayed updating of image translation. Fruit flies appear to interrelate self-motion and its visual feedback within a surprisingly long time window of about 2 s.
Here, we explore a method to directly assess the relevance of the various currents for electrolocation. In this new method, the pattern of current flow during a gymnotid EOD is changed selectively at distinct phases of the EOD so that currents generated by known electrocyte groups are affected.
We report that the archer fish can predict the point where the dislodged prey will later hit the water surface and move in a straight line towards that point, thus enabling it to arrive as fast as possible. Only about 100 ms after prey is dislodged, the fish initiate a quick turn that aligns their body axis right towards where the prey will later land, and not to the actual position of the prey at that moment.
Gymnotiform weakly electric fish find their way in the dark using a continuously operating active sensory system. An electric organ generates a continuous train of discharges (electric organ discharges, EODs), and tuberous high-frequency electroreceptors monitor the pattern of transcutaneous current flow associated with each EOD. Here, I report that a prior interruption to the continuous train of EODs dramatically affects a response shown by many pulse-type gymnotids. (...) These findings show that continuous activity is required either to maintain sensitivity to high-frequency electrical stimuli or to ensure that such stimuli are able to modulate efficiently the pacemaker that sets the discharge frequency.
Several insects use template-matching systems to recognize objects or environmental landmarks by comparing actual and stored retinal images. Such systems are not viewpoint-invariant and are useful only when the locations in which the images have been stored and where they are later retrieved coincide. Here, we describe that a vertebrate, the weakly electric fish Gnathonemus petersii, appears to use template-matching to recognize visual patterns that it had previously viewed from a fixed vantage point. This fish is nocturnal and uses its electrical sense to find its way in the dark, yet it has functional vision that appears to be well adapted to dim light conditions. We were able to train three fish in a two- alternative forced-choice procedure to discriminate a rewarded from an unrewarded visual pattern. From its daytime shelter, each fish viewed two visual patterns placed at a set distance behind a transparent Plexiglas screen that closed the shelter. When the screen was lifted, the fish swam towards one of the patterns to receive a food reward or to be directed back into its shelter. Successful pattern discrimination was limited to low ambient light intensities of approximately 10lx and to pattern sizes subtending a visual angle greater than 3°. To analyze the characteristics used by the fish to discriminate the visual training patterns, we performed transfer tests in which the training patterns were replaced by other patterns. The results of all such transfer tests can best be explained by a template-matching mechanism in which the fish stores the view of the rewarded training pattern and chooses from two other patterns the one whose retinal appearance best matches the stored view.
Weakly electric fish of the pulse type electrolocate objects in the dark by emitting discrete electric organ discharges (EODs) separated by intervals of silence. Two neighbouring pulse-type fish often reduce the risk of discharging simultaneously by means of an ‘echo response’: one fish will respond to a neighbour’s EOD with a discharge of its own following at a fixed short latency so that its EOD will occur long before the next EOD of its neighbour. Although working elegantly for two partners, this simple strategy should fail in larger groups because two fish could discharge in response to the same EOD of a third fish. Here, I show that the mormyrid fish Gnathonemus petersii could use a simple mechanism to reduce this problem.
During their entire lives, weakly electric fish produce an uninterrupted train of discharges to electrolocate objects and to communicate. In an attempt to learn about activity- dependent processes that might be involved in this ability, the continuous train of discharges of intact Gymnotus carapo was experimentally interrupted to investigate how this pausing affects post-pause electric organ discharges. In particular, an analysis was conducted of how the amplitude and relative timing of the three major deflections of the complex discharge change over the course of the first 1000 post-pause discharges...
A computerized 360 ° panorama allowed us to suppress most of the locomotion-induced visual feedback of a freely walking fly without neutralizing its mechanosensory system (‘virtual open-loop’ conditions). This novel paradigm achieves control over the fly’s visual input by continuously evaluating its actual position and orientation.
Thermal noise is known to cause a finite resistance Rp of over damped Josephson junctions even in the zero-current limit. By extending the treatment of Ambegaokar and Halperin the magnetic-field dependence of this resistance is analyzed for arbitrary current-phase relations. We show that the measurement of the magnetic-field dependence of Rp allows the determination of the magnetic-field dependence of the critical current in the temperature regime where thermal-noise rounding effects prevent the application of the usual methods. Applying this technique the correlation function of the super current distribution of YBa2Cu3O7-d grain-boundary junctions could be determined with a spatial resolution of 130 nm.