Sensorimotor adaptation to destabilizing dynamics in weakly electric fish.

Humans and other animals can readily learn to compensate for changes in the dynamics of movement. Such changes can result from an injury or changes in the weight of carried objects. These changes in dynamics can lead not only to reduced performance but also to dramatic instabilities. We evaluated the impacts of compensatory changes in control policies in relation to stability and robustness in Eigenmannia virescens, a species of weakly electric fish. We discovered that these fish retune their sensorimotor control system in response to experimentally generated destabilizing dynamics. Specifically, we used an augmented reality system to manipulate sensory feedback during an image stabilization task in which a fish maintained its position within a refuge. The augmented reality system measured the fish's movements in real time. These movements were passed through a high-pass filter and multiplied by a gain factor before being fed back to the refuge motion. We adjusted the gain factor to gradually destabilize the fish's sensorimotor loop. The fish retuned their sensorimotor control system to compensate for the experimentally induced destabilizing dynamics. This retuning was partially maintained when the augmented reality feedback was abruptly removed. The compensatory changes in sensorimotor control improved tracking performance as well as control-theoretic measures of robustness, including reduced sensitivity to disturbances and improved phase margins.

Corrigendum: Neural mechanisms for turn-taking in duetting plain-tailed wrens.

[This corrects the article DOI: 10.3389/fncir.2022.970434.].

Neural mechanisms for turn-taking in duetting plain-tailed wrens.

Recent studies conducted in the natural habitats of songbirds have provided new insights into the neural mechanisms of turn-taking. For example, female and male plain-tailed wrens (Pheugopedius euophrys) sing a duet that is so precisely timed it sounds as if a single bird is singing. In this review, we discuss our studies examining the sensory and motor cues that pairs of wrens use to coordinate the rapid alternation of syllable production. Our studies included behavioral measurements of freely-behaving wrens in their natural habitat and neurophysiological experiments conducted in awake and anesthetized individuals at field sites in Ecuador. These studies show that each partner has a pattern-generating circuit in their brain that is linked via acoustic feedback between individuals. A similar control strategy has been described in another species of duetting songbird, white-browed sparrow-weavers (Plocepasser mahali). Interestingly, the combination of neurophysiological results from urethane-anesthetized and awake wrens suggest a role for inhibition in coordinating the timing of turn-taking. Finally, we highlight some of the unique challenges of conducting these experiments at remote field sites.

Neurophysiological coordination of duet singing.

Coordination of behavior for cooperative performances often relies on linkages mediated by sensory cues exchanged between participants. How neurophysiological responses to sensory information affect motor programs to coordinate behavior between individuals is not known. We investigated how plain-tailed wrens (Pheugopedius euophrys) use acoustic feedback to coordinate extraordinary duet performances in which females and males rapidly take turns singing. We made simultaneous neurophysiological recordings in a song control area "HVC" in pairs of singing wrens at a field site in Ecuador. HVC is a premotor area that integrates auditory feedback and is necessary for song production. We found that spiking activity of HVC neurons in each sex increased for production of its own syllables. In contrast, hearing sensory feedback produced by the bird's partner decreased HVC activity during duet singing, potentially coordinating HVC premotor activity in each bird through inhibition. When birds sang alone, HVC neurons in females but not males were inhibited by hearing the partner bird. When birds were anesthetized with urethane, which antagonizes GABAergic (γ-aminobutyric acid) transmission, HVC neurons were excited rather than inhibited, suggesting a role for GABA in the coordination of duet singing. These data suggest that HVC integrates information across partners during duets and that rapid turn taking may be mediated, in part, by inhibition.

Spooky Interaction at a Distance in Cave and Surface Dwelling Electric Fishes.

Glass knifefish (Eigenmannia) are a group of weakly electric fishes found throughout the Amazon basin. Their electric organ discharges (EODs) are energetically costly adaptations used in social communication and for localizing conspecifics and other objects including prey at night and in turbid water. Interestingly, a troglobitic population of blind cavefish Eigenmannia vicentespelea survives in complete darkness in a cave system in central Brazil. We examined the effects of troglobitic conditions, which includes a complete loss of visual cues and potentially reduced food sources, by comparing the behavior and movement of freely behaving cavefish to a nearby epigean (surface) population (Eigenmannia trilineata). We found that the strengths of electric discharges in cavefish were greater than in surface fish, which may result from increased reliance on electrosensory perception, larger size, and sufficient food resources. Surface fish were recorded while feeding at night and did not show evidence of territoriality, whereas cavefish appeared to maintain territories. Surprisingly, we routinely found both surface and cavefish with sustained differences in EOD frequencies that were below 10 Hz despite being within close proximity of about 50 cm. A half century of analysis of electrosocial interactions in laboratory tanks suggest that these small differences in EOD frequencies should have triggered the "jamming avoidance response," a behavior in which fish change their EOD frequencies to increase the difference between individuals. Pairs of fish also showed significant interactions between EOD frequencies and relative movements at large distances, over 1.5 m, and at high differences in frequencies, often >50 Hz. These interactions are likely "envelope" responses in which fish alter their EOD frequency in relation to higher order features, specifically changes in the depth of modulation, of electrosocial signals.

Variability in locomotor dynamics reveals the critical role of feedback in task control.

Animals vary considerably in size, shape, and physiological features across individuals, but yet achieve remarkably similar behavioral performances. We examined how animals compensate for morphophysiological variation by measuring the system dynamics of individual knifefish (Eigenmannia virescens) in a refuge tracking task. Kinematic measurements of Eigenmannia were used to generate individualized estimates of each fish's locomotor plant and controller, revealing substantial variability between fish. To test the impact of this variability on behavioral performance, these models were used to perform simulated 'brain transplants'-computationally swapping controllers and plants between individuals. We found that simulated closed-loop performance was robust to mismatch between plant and controller. This suggests that animals rely on feedback rather than precisely tuned neural controllers to compensate for morphophysiological variability.

People come in different shapes and sizes, but most will perform similarly well if asked to complete a task requiring fine manual dexterity ­ such as holding a pen or picking up a single grape. How can different individuals, with different sized hands and muscles, produce such similar movements? One explanation is that an individual's brain and nervous system become precisely tuned to mechanics of the body's muscles and skeleton. An alternative explanation is that brain and nervous system use a more "robust" control policy that can compensate for differences in the body by relying on feedback from the senses to guide the movements. To distinguish between these two explanations, Uyanik et al. turned to weakly electric freshwater fish known as glass knifefish. These fish seek refuge within root systems, reed grass and among other objects in the water. They swim backwards and forwards to stay hidden despite constantly changing currents. Each fish shuttles back and forth by moving a long ribbon-like fin on the underside of its body. Uyanik et al. measured the movements of the ribbon fin under controlled conditions in the laboratory, and then used the data to create computer models of the brain and body of each fish. The models of each fish's brain and body were quite different. To study how the brain interacts with the body, Uyanik et al. then conducted experiments reminiscent of those described in the story of Frankenstein and transplanted the brain from each computer model into the body of different model fish. These "brain swaps" had almost no effect on the model's simulated swimming behavior. Instead, these "Frankenfish" used sensory feedback to compensate for any mismatch between their brain and body. This suggests that, for some behaviors, an animal's brain does not need to be precisely tuned to the specific characteristics of its body. Instead, robust control of movement relies on many seemingly redundant systems that provide sensory feedback. This has implications for the field of robotics. It further suggests that when designing robots, engineers should prioritize enabling the robots to use sensory feedback to cope with unexpected events, a well-known idea in control engineering.

From Perception to Action: The Role of Auditory Input in Shaping Vocal Communication and Social Behaviors in Birds.

Acoustic communication signals are typically generated to influence the behavior of conspecific receivers. In songbirds, for instance, such cues are routinely used by males to influence the behavior of females and rival males. There is remarkable diversity in vocalizations across songbird species, and the mechanisms of vocal production have been studied extensively, yet there has been comparatively little emphasis on how the receiver perceives those signals and uses that information to direct subsequent actions. Here, we emphasize the receiver as an active participant in the communication process. The roles of sender and receiver can alternate between individuals, resulting in an emergent feedback loop that governs the behavior of both. We describe three lines of research that are beginning to reveal the neural mechanisms that underlie the reciprocal exchange of information in communication. These lines of research focus on the perception of the repertoire of songbird vocalizations, evaluation of vocalizations in mate choice, and the coordination of duet singing.

Sensory Cues Modulate Smooth Pursuit and Active Sensing Movements.

Animals routinely use autogenous movement to regulate the information encoded by their sensory systems. Weakly electric fish use fore-aft movements to regulate visual and electrosensory feedback as they maintain position within a moving refuge. During refuge tracking, fish produce two categories of movements: smooth pursuit that is approximately linear in its relation to the movement of the refuge and ancillary active sensing movements that are nonlinear. We identified four categories of nonlinear movements which we termed scanning, wiggle, drift, and reset. To examine the relations between sensory cues and production of both linear smooth pursuit and nonlinear active sensing movements, we altered visual and electrosensory cues for refuge tracking and measured the fore-aft movements of the fish. Specifically, we altered the length and structure of the refuge and performed experiments with light and in complete darkness. Linear measures of tracking performance were better for shorter refuges (less than a body length) than longer ones (>1.5 body lengths). The magnitude of nonlinear active sensing movements was strongly modulated by light cues but also increased as a function of both longer refuge length and decreased features. Specifically, fish shifted swimming movements from smooth pursuit to scanning when tracking in dark conditions. Finally, fish appear to use nonlinear movements as an alternate tracking strategy in longer refuges: the fish may use more drifts and resets to avoid exiting the ends of the refuge.

Closed-Loop Control of Active Sensing Movements Regulates Sensory Slip.

Active sensing involves the production of motor signals for the purpose of acquiring sensory information [1-3]. The most common form of active sensing, found across animal taxa and behaviors, involves the generation of movements-e.g., whisking [4-6], touching [7, 8], sniffing [9, 10], and eye movements [11]. Active sensing movements profoundly affect the information carried by sensory feedback pathways [12-15] and are modulated by both top-down goals (e.g., measuring weight versus texture [1, 16]) and bottom-up stimuli (e.g., lights on or off [12]), but it remains unclear whether and how these movements are controlled in relation to the ongoing feedback they generate. To investigate the control of movements for active sensing, we created an experimental apparatus for freely swimming weakly electric fish, Eigenmannia virescens, that modulates the gain of reafferent feedback by adjusting the position of a refuge based on real-time videographic measurements of fish position. We discovered that fish robustly regulate sensory slip via closed-loop control of active sensing movements. Specifically, as fish performed the task of maintaining position inside the refuge [17-22], they dramatically up- or downregulated fore-aft active sensing movements in relation to a 4-fold change of experimentally modulated reafferent gain. These changes in swimming movements served to maintain a constant magnitude of sensory slip. The magnitude of sensory slip depended on the presence or absence of visual cues. These results indicate that fish use two controllers: one that controls the acquisition of information by regulating feedback from active sensing movements and another that maintains position in the refuge, a control structure that may be ubiquitous in animals [23, 24].

High-resolution behavioral mapping of electric fishes in Amazonian habitats.

The study of animal behavior has been revolutionized by sophisticated methodologies that identify and track individuals in video recordings. Video recording of behavior, however, is challenging for many species and habitats including fishes that live in turbid water. Here we present a methodology for identifying and localizing weakly electric fishes on the centimeter scale with subsecond temporal resolution based solely on the electric signals generated by each individual. These signals are recorded with a grid of electrodes and analyzed using a two-part algorithm that identifies the signals from each individual fish and then estimates the position and orientation of each fish using Bayesian inference. Interestingly, because this system involves eavesdropping on electrocommunication signals, it permits monitoring of complex social and physical interactions in the wild. This approach has potential for large-scale non-invasive monitoring of aquatic habitats in the Amazon basin and other tropical freshwater systems.

Dynamic modulation of visual and electrosensory gains for locomotor control.

Animal nervous systems resolve sensory conflict for the control of movement. For example, the glass knifefish, Eigenmannia virescens, relies on visual and electrosensory feedback as it swims to maintain position within a moving refuge. To study how signals from these two parallel sensory streams are used in refuge tracking, we constructed a novel augmented reality apparatus that enables the independent manipulation of visual and electrosensory cues to freely swimming fish (n = 5). We evaluated the linearity of multisensory integration, the change to the relative perceptual weights given to vision and electrosense in relation to sensory salience, and the effect of the magnitude of sensory conflict on sensorimotor gain. First, we found that tracking behaviour obeys superposition of the sensory inputs, suggesting linear sensorimotor integration. In addition, fish rely more on vision when electrosensory salience is reduced, suggesting that fish dynamically alter sensorimotor gains in a manner consistent with Bayesian integration. However, the magnitude of sensory conflict did not significantly affect sensorimotor gain. These studies lay the theoretical and experimental groundwork for future work investigating multisensory control of locomotion.

Reproductive state modulates testosterone-induced singing in adult female European starlings (Sturnus vulgaris).

European starlings (Sturnus vulgaris) exhibit seasonal changes in singing and in the volumes of the neural substrate. Increases in song nuclei volume are mediated at least in part by increases in day length, which is also associated with increases in plasma testosterone (T), reproductive activity, and singing behavior in males. The correlations between photoperiod (i.e. daylength), T, reproductive state and singing hamper our ability to disentangle causal relationships. We investigated how photoperiodic-induced variation in reproductive state modulates the effects of T on singing behavior and song nuclei volumes in adult female starlings. Female starlings do not naturally produce measureable levels of circulating T but nevertheless respond to exogenous T, which induces male-like singing. We manipulated photoperiod by placing birds in a photosensitive or photorefractory state and then treated them with T-filled or empty silastic implants. We recorded morning singing behavior for 3 weeks, after which we assessed reproductive condition and measured song nuclei volumes. We found that T-treated photosensitive birds sang significantly more than all other groups including T-treated photorefractory birds. All T-treated birds had larger song nuclei volumes than with blank-treated birds (despite photorefractory T-treated birds not increasing song-rate). There was no effect of photoperiod on the song nuclei volumes of T-treated birds. These data show that the behavioral effects of exogenous T can be modulated by reproductive state in adult female songbirds. Furthermore, these data are consistent with other observations that increases in singing rate in response to T are not necessarily due to the direct effects of T on song nuclei volume.

Feedback control as a framework for understanding tradeoffs in biology.

Control theory arose from a need to control synthetic systems. From regulating steam engines to tuning radios to devices capable of autonomous movement, it provided a formal mathematical basis for understanding the role of feedback in the stability (or change) of dynamical systems. It provides a framework for understanding any system with regulation via feedback, including biological ones such as regulatory gene networks, cellular metabolic systems, sensorimotor dynamics of moving animals, and even ecological or evolutionary dynamics of organisms and populations. Here, we focus on four case studies of the sensorimotor dynamics of animals, each of which involves the application of principles from control theory to probe stability and feedback in an organism's response to perturbations. We use examples from aquatic (two behaviors performed by electric fish), terrestrial (following of walls by cockroaches), and aerial environments (flight control by moths) to highlight how one can use control theory to understand the way feedback mechanisms interact with the physical dynamics of animals to determine their stability and response to sensory inputs and perturbations. Each case study is cast as a control problem with sensory input, neural processing, and motor dynamics, the output of which feeds back to the sensory inputs. Collectively, the interaction of these systems in a closed loop determines the behavior of the entire system.

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.

Closed-loop stabilization of the Jamming Avoidance Response reveals its locally unstable and globally nonlinear dynamics.

The Jamming Avoidance Response, or JAR, in the weakly electric fish has been analyzed at all levels of organization, from whole-organism behavior down to specific ion channels. Nevertheless, a parsimonious description of the JAR behavior in terms of a dynamical system model has not been achieved at least in part due to the fact that 'avoidance' behaviors are both intrinsically unstable and nonlinear. We overcame the instability of the JAR in Eigenmannia virescens by closing a feedback loop around the behavioral response of the animal. Specifically, the instantaneous frequency of a jamming stimulus was tied to the fish's own electrogenic frequency by a feedback law. Without feedback, the fish's own frequency diverges from the stimulus frequency, but appropriate feedback stabilizes the behavior. After stabilizing the system, we measured the responses in the fish's instantaneous frequency to various stimuli. A delayed first-order linear system model fitted the behavior near the equilibrium. Coherence to white noise stimuli together with quantitative agreement across stimulus types supported this local linear model. Next, we examined the intrinsic nonlinearity of the behavior using clamped frequency difference experiments to extend the model beyond the neighborhood of the equilibrium. The resulting nonlinear model is composed of competing motor return and sensory escape terms. The model reproduces responses to step and ramp changes in the difference frequency (df) and predicts a 'snap-through' bifurcation as a function of dF that we confirmed experimentally.

Perception and coding of envelopes in weakly electric fishes.

Natural sensory stimuli have a rich spatiotemporal structure and can often be characterized as a high frequency signal that is independently modulated at lower frequencies. This lower frequency modulation is known as the envelope. Envelopes are commonly found in a variety of sensory signals, such as contrast modulations of visual stimuli and amplitude modulations of auditory stimuli. While psychophysical studies have shown that envelopes can carry information that is essential for perception, how envelope information is processed in the brain is poorly understood. Here we review the behavioral salience and neural mechanisms for the processing of envelopes in the electrosensory system of wave-type gymnotiform weakly electric fishes. These fish can generate envelope signals through movement, interactions of their electric fields in social groups or communication signals. The envelopes that result from the first two behavioral contexts differ in their frequency content, with movement envelopes typically being of lower frequency. Recent behavioral evidence has shown that weakly electric fish respond in robust and stereotypical ways to social envelopes to increase the envelope frequency. Finally, neurophysiological results show how envelopes are processed by peripheral and central electrosensory neurons. Peripheral electrosensory neurons respond to both stimulus and envelope signals. Neurons in the primary hindbrain recipient of these afferents, the electrosensory lateral line lobe (ELL), exhibit heterogeneities in their responses to stimulus and envelope signals. Complete segregation of stimulus and envelope information is achieved in neurons in the target of ELL efferents, the midbrain torus semicircularis (Ts).

Beyond the Jamming Avoidance Response: weakly electric fish respond to the envelope of social electrosensory signals.

Recent studies have shown that central nervous system neurons in weakly electric fish respond to artificially constructed electrosensory envelopes, but the behavioral relevance of such stimuli is unclear. Here we investigate the possibility that social context creates envelopes that drive behavior. When Eigenmannia virescens are in groups of three or more, the interactions between their pseudo-sinusoidal electric fields can generate 'social envelopes'. We developed a simple mathematical prediction for how fish might respond to such social envelopes. To test this prediction, we measured the responses of E. virescens to stimuli consisting of two sinusoids, each outside the range of the Jamming Avoidance Response (JAR), that when added to the fish's own electric field produced low-frequency (below 10 Hz) social envelopes. Fish changed their electric organ discharge (EOD) frequency in response to these envelopes, which we have termed the Social Envelope Response (SER). In 99% of trials, the direction of the SER was consistent with the mathematical prediction. The SER was strongest in response to the lowest initial envelope frequency tested (2 Hz) and depended on stimulus amplitude. The SER generally resulted in an increase of the envelope frequency during the course of a trial, suggesting that this behavior may be a mechanism for avoiding low-frequency social envelopes. Importantly, the direction of the SER was not predicted by the superposition of two JAR responses: the SER was insensitive to the amplitude ratio between the sinusoids used to generate the envelope, but was instead predicted by the sign of the difference of difference frequencies.

Active sensing via movement shapes spatiotemporal patterns of sensory feedback.

Previous work has shown that animals alter their locomotor behavior to increase sensing volumes. However, an animal's own movement also determines the spatial and temporal dynamics of sensory feedback. Because each sensory modality has unique spatiotemporal properties, movement has differential and potentially independent effects on each sensory system. Here we show that weakly electric fish dramatically adjust their locomotor behavior in relation to changes of modality-specific information in a task in which increasing sensory volume is irrelevant. We varied sensory information during a refuge-tracking task by changing illumination (vision) and conductivity (electroreception). The gain between refuge movement stimuli and fish tracking responses was functionally identical across all sensory conditions. However, there was a significant increase in the tracking error in the dark (no visual cues). This was a result of spontaneous whole-body oscillations (0.1 to 1 Hz) produced by the fish. These movements were costly: in the dark, fish swam over three times further when tracking and produced more net positive mechanical work. The magnitudes of these oscillations increased as electrosensory salience was degraded via increases in conductivity. In addition, tail bending (1.5 to 2.35 Hz), which has been reported to enhance electrosensory perception, occurred only during trials in the dark. These data show that both categories of movements - whole-body oscillations and tail bends - actively shape the spatiotemporal dynamics of electrosensory feedback.

Parallel coding of first- and second-order stimulus attributes by midbrain electrosensory neurons.

Natural stimuli often have time-varying first-order (i.e., mean) and second-order (i.e., variance) attributes that each carry critical information for perception and can vary independently over orders of magnitude. Experiments have shown that sensory systems continuously adapt their responses based on changes in each of these attributes. This adaptation creates ambiguity in the neural code as multiple stimuli may elicit the same neural response. While parallel processing of first- and second-order attributes by separate neural pathways is sufficient to remove this ambiguity, the existence of such pathways and the neural circuits that mediate their emergence have not been uncovered to date. We recorded the responses of midbrain electrosensory neurons in the weakly electric fish Apteronotus leptorhynchus to stimuli with first- and second-order attributes that varied independently in time. We found three distinct groups of midbrain neurons: the first group responded to both first- and second-order attributes, the second group responded selectively to first-order attributes, and the last group responded selectively to second-order attributes. In contrast, all afferent hindbrain neurons responded to both first- and second-order attributes. Using computational analyses, we show how inputs from a heterogeneous population of ON- and OFF-type afferent neurons are combined to give rise to response selectivity to either first- or second-order stimulus attributes in midbrain neurons. Our study thus uncovers, for the first time, generic and widely applicable mechanisms by which parallel processing of first- and second-order stimulus attributes emerges in the brain.