A robot-rodent interaction arena with adjustable spatial complexity for ethologically relevant behavioral studies.

Outside of the laboratory, animals behave in spaces where they can transition between open areas and coverage as they interact with others. Replicating these conditions in the laboratory can be difficult to control and record. This has led to a dominance of relatively simple, static behavioral paradigms that reduce the ethological relevance of behaviors and may alter the engagement of cognitive processes such as planning and decision-making. Therefore, we developed a method for controllable, repeatable interactions with others in a reconfigurable space. Mice navigate a large honeycomb lattice of adjustable obstacles as they interact with an autonomous robot coupled to their actions. We illustrate the system using the robot as a pseudo-predator, delivering airpuffs to the mice. The combination of obstacles and a mobile threat elicits a diverse set of behaviors, such as increased path diversity, peeking, and baiting, providing a method to explore ethologically relevant behaviors in the laboratory.

Evolution: Blinking through deep time.

Terrestrial vertebrates blink, but most aquatic vertebrates do not. How and why did blinking evolve? A recent study looks at this through the eyes of a mudskipper, fish that stay on land for long periods and blink.

Spinal Basis of Direction Control during Locomotion in Larval Zebrafish.

Navigation requires steering and propulsion, but how spinal circuits contribute to direction control during ongoing locomotion is not well understood. Here, we use drifting vertical gratings to evoke directed "fictive" swimming in intact but immobilized larval zebrafish while performing electrophysiological recordings from spinal neurons. We find that directed swimming involves unilateral changes in the duration of motor output and increased recruitment of motor neurons, without impacting the timing of spiking across or along the body. Voltage-clamp recordings from motor neurons reveal increases in phasic excitation and inhibition on the side of the turn. Current-clamp recordings from premotor interneurons that provide phasic excitation or inhibition reveal two types of recruitment patterns. A direction-agnostic pattern with balanced recruitment on the turning and nonturning sides is primarily observed in excitatory V2a neurons with ipsilateral descending axons, while a direction-sensitive pattern with preferential recruitment on the turning side is dominated by V2a neurons with ipsilateral bifurcating axons. Inhibitory V1 neurons are also divided into direction-sensitive and direction-agnostic subsets, although there is no detectable morphologic distinction. Our findings support the modular control of steering and propulsion by spinal premotor circuits, where recruitment of distinct subsets of excitatory and inhibitory interneurons provide adjustments in direction while on the move.SIGNIFICANCE STATEMENT Spinal circuits play an essential role in coordinating movements during locomotion. However, it is unclear how they participate in adjustments in direction that do not interfere with coordination. Here we have developed a system using larval zebrafish that allows us to directly record electrical signals from spinal neurons during "fictive" swimming guided by visual cues. We find there are subsets of spinal interneurons for coordination and others that drive unilateral asymmetries in motor neuron recruitment for direction control. Our findings suggest a modular organization of spinal premotor circuits that enables uninterrupted adjustments in direction during ongoing locomotion.

The neuroecology of the water-to-land transition and the evolution of the vertebrate brain.

The water-to-land transition in vertebrate evolution offers an unusual opportunity to consider computational affordances of a new ecology for the brain. All sensory modalities are changed, particularly a greatly enlarged visual sensorium owing to air versus water as a medium, and expanded by mobile eyes and neck. The multiplication of limbs, as evolved to exploit aspects of life on land, is a comparable computational challenge. As the total mass of living organisms on land is a hundredfold larger than the mass underwater, computational improvements promise great rewards. In water, the midbrain tectum coordinates approach/avoid decisions, contextualized by water flow and by the animal's body state and learning. On land, the relative motions of sensory surfaces and effectors must be resolved, adding on computational architectures from the dorsal pallium, such as the parietal cortex. For the large-brained and long-living denizens of land, making the right decision when the wrong one means death may be the basis of planning, which allows animals to learn from hypothetical experience before enactment. Integration of value-weighted, memorized panoramas in basal ganglia/frontal cortex circuitry, with allocentric cognitive maps of the hippocampus and its associated cortices becomes a cognitive habit-to-plan transition as substantial as the change in ecology. This article is part of the theme issue 'Systems neuroscience through the lens of evolutionary theory'.

Intersection of motor volumes predicts the outcome of ambush predation of larval zebrafish.

Escape maneuvers are key determinants of animal survival and are under intense selection pressure. A number of escape maneuver parameters contribute to survival, including response latency, escape speed and direction. However, the relative importance of these parameters is context dependent, suggesting that interactions between parameters and predatory context determine the likelihood of escape success. To better understand how escape maneuver parameters interact and contribute to survival, we analyzed the responses of larval zebrafish (Danio rerio) to the attacks of dragonfly nymphs (Sympetrum vicinum). We found that no single parameter explains the outcome. Instead, the relative intersection of the swept volume of the nymph's grasping organs with the volume containing all possible escape trajectories of the fish is the strongest predictor of escape success. In cases where the prey's motor volume exceeds that of the predator, the prey survives. By analyzing the intersection of these volumes, we compute the survival benefit of recruiting the Mauthner cell, a neuron in anamniotes devoted to producing escapes. We discuss how the intersection of motor volume approach provides a framework that unifies the influence of many escape maneuver parameters on the likelihood of survival.

Tuning movement for sensing in an uncertain world.

While animals track or search for targets, sensory organs make small unexplained movements on top of the primary task-related motions. While multiple theories for these movements exist-in that they support infotaxis, gain adaptation, spectral whitening, and high-pass filtering-predicted trajectories show poor fit to measured trajectories. We propose a new theory for these movements called energy-constrained proportional betting, where the probability of moving to a location is proportional to an expectation of how informative it will be balanced against the movement's predicted energetic cost. Trajectories generated in this way show good agreement with measured trajectories of fish tracking an object using electrosense, a mammal and an insect localizing an odor source, and a moth tracking a flower using vision. Our theory unifies the metabolic cost of motion with information theory. It predicts sense organ movements in animals and can prescribe sensor motion for robots to enhance performance.

Publisher Correction: Spatial planning with long visual range benefits escape from visual predators in complex naturalistic environments.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Spatial planning with long visual range benefits escape from visual predators in complex naturalistic environments.

It is uncontroversial that land animals have more elaborated cognitive abilities than their aquatic counterparts such as fish. Yet there is no apparent a-priori reason for this. A key cognitive faculty is planning. We show that in visually guided predator-prey interactions, planning provides a significant advantage, but only on land. During animal evolution, the water-to-land transition resulted in a massive increase in visual range. Simulations of behavior identify a specific type of terrestrial habitat, clustered open and closed areas (savanna-like), where the advantage of planning peaks. Our computational experiments demonstrate how this patchy terrestrial structure, in combination with enhanced visual range, can reveal and hide agents as a function of their movement and create a selective benefit for imagining, evaluating, and selecting among possible future scenarios-in short, for planning. The vertebrate invasion of land may have been an important step in their cognitive evolution.

Visual Threat Assessment and Reticulospinal Encoding of Calibrated Responses in Larval Zebrafish.

All visual animals must decide whether approaching objects are a threat. Our current understanding of this process has identified a proximity-based mechanism where an evasive maneuver is triggered when a looming stimulus passes a subtended visual angle threshold. However, some escape strategies are more costly than others, and so it would be beneficial to additionally encode the level of threat conveyed by the predator's approach rate to select the most appropriate response. Here, using naturalistic rates of looming visual stimuli while simultaneously monitoring escape behavior and the recruitment of multiple reticulospinal neurons, we find that larval zebrafish do indeed perform a calibrated assessment of threat. While all fish generate evasive maneuvers at the same subtended visual angle, lower approach rates evoke slower, more kinematically variable escape responses with relatively long latencies as well as the unilateral recruitment of ventral spinal projecting nuclei (vSPNs) implicated in turning. In contrast, higher approach rates evoke faster, more kinematically stereotyped responses with relatively short latencies, as well as bilateral recruitment of vSPNs and unilateral recruitment of giant fiber neurons in fish and amphibians called Mauthner cells. In addition to the higher proportion of more costly, shorter-latency Mauthner-active responses to greater perceived threats, we observe a higher incidence of freezing behavior at higher approach rates. Our results provide a new framework to understand how behavioral flexibility is grounded in the appropriate balancing of trade-offs between fast and slow movements when deciding to respond to a visually perceived threat.

Massive increase in visual range preceded the origin of terrestrial vertebrates.

The evolution of terrestrial vertebrates, starting around 385 million years ago, is an iconic moment in evolution that brings to mind images of fish transforming into four-legged animals. Here, we show that this radical change in body shape was preceded by an equally dramatic change in sensory abilities akin to transitioning from seeing over short distances in a dense fog to seeing over long distances on a clear day. Measurements of eye sockets and simulations of their evolution show that eyes nearly tripled in size just before vertebrates began living on land. Computational simulations of these animal's visual ecology show that for viewing objects through water, the increase in eye size provided a negligible increase in performance. However, when viewing objects through air, the increase in eye size provided a large increase in performance. The jump in eye size was, therefore, unlikely to have arisen for seeing through water and instead points to an unexpected hybrid of seeing through air while still primarily inhabiting water. Our results and several anatomical innovations arising at the same time suggest lifestyle similarity to crocodiles. The consequent combination of the increase in eye size and vision through air would have conferred a 1 million-fold increase in the amount of space within which objects could be seen. The "buena vista" hypothesis that our data suggest is that seeing opportunities from afar played a role in the subsequent evolution of fully terrestrial limbs as well as the emergence of elaborated action sequences through planning circuits in the nervous system.

Neuroscience Needs Behavior: Correcting a Reductionist Bias.

There are ever more compelling tools available for neuroscience research, ranging from selective genetic targeting to optogenetic circuit control to mapping whole connectomes. These approaches are coupled with a deep-seated, often tacit, belief in the reductionist program for understanding the link between the brain and behavior. The aim of this program is causal explanation through neural manipulations that allow testing of necessity and sufficiency claims. We argue, however, that another equally important approach seeks an alternative form of understanding through careful theoretical and experimental decomposition of behavior. Specifically, the detailed analysis of tasks and of the behavior they elicit is best suited for discovering component processes and their underlying algorithms. In most cases, we argue that study of the neural implementation of behavior is best investigated after such behavioral work. Thus, we advocate a more pluralistic notion of neuroscience when it comes to the brain-behavior relationship: behavioral work provides understanding, whereas neural interventions test causality.

Human-in-the-loop active electrosense.

Active electrosense is a non-visual, short range sensing system used by weakly electric fish, enabling such fish to locate and identify objects in total darkness. Here we report initial findings from the use of active electrosense for object localization during underwater teleoperation with a virtual reality (VR) head-mounted display (HMD). The advantage of electrolocating with a VR system is that it naturally allows for aspects of the task that are difficult for a person to perform to be allocated to the computer. However, interpreting weak and incomplete patterns in the incoming data is something that people are typically far better at than computers. To achieve human-computer synergy, we integrated an active electrosense underwater robot with the Oculus Rift HMD. The virtual environment contains a visualization of the electric images of the objects surrounding the robot as well as various virtual fixtures that guide users to regions of higher information value. Initial user testing shows that these fixtures significantly reduce the time taken to localize an object, but may not increase the accuracy of the position estimate. Our results highlight the advantages of translating the unintuitive physics of electrolocation to an intuitive visual representation for accomplishing tasks in environments where imaging systems fail, such as in dark or turbid water.

Enhanced detection performance in electrosense through capacitive sensing.

Weakly electric fish emit an AC electric field into the water and use thousands of sensors on the skin to detect field perturbations due to surrounding objects. The fish's active electrosensory system allows them to navigate and hunt, using separate neural pathways and receptors for resistive and capacitive perturbations. We have previously developed a sensing method inspired by the weakly electric fish to detect resistive perturbations and now report on an extension of this system to detect capacitive perturbations as well. In our method, an external object is probed by an AC field over multiple frequencies. We present a quantitative framework that relates the response of a capacitive object at multiple frequencies to the object's composition and internal structure, and we validate this framework with an electrosense robot that implements our capacitive sensing method. We define a metric for comparing the electrosensory range of different underwater electrosense systems. For detecting non-conductive objects, we show that capacitive sensing performs better than resistive sensing by almost an order of magnitude using this measure, while for conductive objects there is a four-fold increase in performance. Capacitive sensing could therefore provide electric fish with extended sensing range for capacitive objects such as prey, and gives artificial electrolocation systems enhanced range for targets that are capacitive.

Convergent evolution of mechanically optimal locomotion in aquatic invertebrates and vertebrates.

Examples of animals evolving similar traits despite the absence of that trait in the last common ancestor, such as the wing and camera-type lens eye in vertebrates and invertebrates, are called cases of convergent evolution. Instances of convergent evolution of locomotory patterns that quantitatively agree with the mechanically optimal solution are very rare. Here, we show that, with respect to a very diverse group of aquatic animals, a mechanically optimal method of swimming with elongated fins has evolved independently at least eight times in both vertebrate and invertebrate swimmers across three different phyla. Specifically, if we take the length of an undulation along an animal's fin during swimming and divide it by the mean amplitude of undulations along the fin length, the result is consistently around twenty. We call this value the optimal specific wavelength (OSW). We show that the OSW maximizes the force generated by the body, which also maximizes swimming speed. We hypothesize a mechanical basis for this optimality and suggest reasons for its repeated emergence through evolution.

Separability of drag and thrust in undulatory animals and machines.

For nearly a century, researchers have tried to understand the swimming of aquatic animals in terms of a balance between the forward thrust from swimming movements and drag on the body. Prior approaches have failed to provide a separation of these two forces for undulatory swimmers such as lamprey and eels, where most parts of the body are simultaneously generating drag and thrust. We nonetheless show that this separation is possible, and delineate its fundamental basis in undulatory swimmers. Our approach unifies a vast diversity of undulatory aquatic animals (anguilliform, sub-carangiform, gymnotiform, bal-istiform, rajiform) and provides design principles for highly agile bioinspired underwater vehicles. This approach has practical utility within biology as well as engineering. It is a predictive tool for use in understanding the role of the mechanics of movement in the evolutionary emergence of morphological features relating to locomotion. For example, we demonstrate that the drag-thrust separation framework helps to predict the observed height of the ribbon fin of electric knifefish, a diverse group of neotropical fish which are an important model system in sensory neurobiology. We also show how drag-thrust separation leads to models that can predict the swimming velocity of an organism or a robotic vehicle.

Undulating fins produce off-axis thrust and flow structures.

While wake structures of many forms of swimming and flying are well characterized, the wake generated by a freely swimming undulating fin has not yet been analyzed. These elongated fins allow fish to achieve enhanced agility exemplified by the forward, backward and vertical swimming capabilities of knifefish, and also have potential applications in the design of more maneuverable underwater vehicles. We present the flow structure of an undulating robotic fin model using particle image velocimetry to measure fluid velocity fields in the wake. We supplement the experimental robotic work with high-fidelity computational fluid dynamics, simulating the hydrodynamics of both a virtual fish, whose fin kinematics and fin plus body morphology are measured from a freely swimming knifefish, and a virtual rendering of our robot. Our results indicate that a series of linked vortex tubes is shed off the long edge of the fin as the undulatory wave travels lengthwise along the fin. A jet at an oblique angle to the fin is associated with the successive vortex tubes, propelling the fish forward. The vortex structure bears similarity to the linked vortex ring structure trailing the oscillating caudal fin of a carangiform swimmer, though the vortex rings are distorted because of the undulatory kinematics of the elongated fin.

Mutually opposing forces during locomotion can eliminate the tradeoff between maneuverability and stability.

A surprising feature of animal locomotion is that organisms typically produce substantial forces in directions other than what is necessary to move the animal through its environment, such as perpendicular to, or counter to, the direction of travel. The effect of these forces has been difficult to observe because they are often mutually opposing and therefore cancel out. Indeed, it is likely that these forces do not contribute directly to movement but may serve an equally important role: to simplify and enhance the control of locomotion. To test this hypothesis, we examined a well-suited model system, the glass knifefish Eigenmannia virescens, which produces mutually opposing forces during a hovering behavior that is analogous to a hummingbird feeding from a moving flower. Our results and analyses, which include kinematic data from the fish, a mathematical model of its swimming dynamics, and experiments with a biomimetic robot, demonstrate that the production and differential control of mutually opposing forces is a strategy that generates passive stabilization while simultaneously enhancing maneuverability. Mutually opposing forces during locomotion are widespread across animal taxa, and these results indicate that such forces can eliminate the tradeoff between stability and maneuverability, thereby simplifying neural control.

Biomimetic and bio-inspired robotics in electric fish research.

Weakly electric knifefish have intrigued both biologists and engineers for decades with their unique electrosensory system and agile swimming mechanics. Study of these fish has resulted in models that illuminate the principles behind their electrosensory system and unique swimming abilities. These models have uncovered the mechanisms by which knifefish generate thrust for swimming forward and backward, hovering, and heaving dorsally using a ventral elongated median fin. Engineered active electrosensory models inspired by electric fish allow for close-range sensing in turbid waters where other sensing modalities fail. Artificial electrosense is capable of aiding navigation, detection and discrimination of objects, and mapping the environment, all tasks for which the fish use electrosense extensively. While robotic ribbon fin and artificial electrosense research has been pursued separately to reduce complications that arise when they are combined, electric fish have succeeded in their ecological niche through close coupling of their sensing and mechanical systems. Future integration of electrosense and ribbon fin technology into a knifefish robot should likewise result in a vehicle capable of navigating complex 3D geometries unreachable with current underwater vehicles, as well as provide insights into how to design mobile robots that integrate high bandwidth sensing with highly responsive multidirectional movement.

Visually guided gradation of prey capture movements in larval zebrafish.

A mechanistic understanding of goal-directed behavior in vertebrates is hindered by the relative inaccessibility and size of their nervous systems. Here, we have studied the kinematics of prey capture behavior in a highly accessible vertebrate model organism, the transparent larval zebrafish (Danio rerio), to assess whether they use visual cues to systematically adjust their movements. We found that zebrafish larvae scale the speed and magnitude of turning movements according to the azimuth of one of their standard prey, paramecia. They also bias the direction of subsequent swimming movements based on prey azimuth and select forward or backward movements based on the prey's direction of travel. Once within striking distance, larvae generate either ram or suction capture behaviors depending on their distance from the prey. From our experimental estimations of ocular receptive fields, we ascertained that the ultimate decision to consume prey is likely a function of the progressive vergence of the eyes that places the target in a proximal binocular 'capture zone'. By repeating these experiments in the dark, we demonstrate that paramecia are only consumed if they contact the anterior extremities of larvae, which triggers ocular vergence and tail movements similar to close proximity captures in lit conditions. These observations confirm the importance of vision in the graded movements we observe leading up to capture of more distant prey in the light, and implicate somatosensation in captures in the absence of light. We discuss the implications of these findings for future work on the neural control of visually guided behavior in zebrafish.

Kinematics of the ribbon fin in hovering and swimming of the electric ghost knifefish.

Weakly electric knifefish are exceptionally maneuverable swimmers. In prior work, we have shown that they are able to move their entire body omnidirectionally so that they can rapidly reach prey up to several centimeters away. Consequently, in addition to being a focus of efforts to understand the neural basis of sensory signal processing in vertebrates, knifefish are increasingly the subject of biomechanical analysis to understand the coupling of signal acquisition and biomechanics. Here, we focus on a key subset of the knifefish's omnidirectional mechanical abilities: hovering in place, and swimming forward at variable speed. Using high-speed video and a markerless motion capture system to capture fin position, we show that hovering is achieved by generating two traveling waves, one from the caudal edge of the fin and one from the rostral edge, moving toward each other. These two traveling waves overlap at a nodal point near the center of the fin, cancelling fore-aft propulsion. During forward swimming at low velocities, the caudal region of the fin continues to have counter-propagating waves, directly retarding forward movement. The gait transition from hovering to forward swimming is accompanied by a shift in the nodal point toward the caudal end of the fin. While frequency varies significantly to increase speed at low velocities, beyond approximately one body length per second, the frequency stays near 10 Hz, and amplitude modulation becomes more prominent. A coupled central pattern generator model is able to reproduce qualitative features of fin motion and suggest hypotheses regarding the fin's neural control.