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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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

The Jamming Avoidance Response, or JAR, in the weakly electric fish has been analyzed at all levels of organization, from wholeorganism 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. [ABSTRACT FROM AUTHOR]

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). [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

The weakly electric glass knifefish, Elgenmannia virescens, will swim forward and backward, using propulsion from an anal ribbon fin, in response to motion of a computer-controlled moving refuge. Fish were recorded performing a refuge-tracking behavior for sinusoidal (predictable) and sum-of-sines (pseudo-random) refuge trajectories. For all trials, we observed high coherence between refuge and fish trajectories, suggesting linearity of the tracking dynamics. But superposition failed: we observed categorical differences in tracking between the predictable single-sine stimuli and the unpredictable sum-of-sines stimuli. This nonlinearity suggests a stimulus-mediated adaptation. At all frequencies tested, fish demonstrated reduced tracking error when tracking single-sine trajectories and this was typically accompanied by a reduction in overall movement. Most notably, fish demonstrated reduced phase lag when tracking single-sine trajectories. These data support the hypothesis that fish generate an internal dynamical model of the stimulus motion, hence improving tracking of predictable trajectories (relative to unpredictable ones) despite similar or reduced motor cost. Similar predictive mechanisms based on the dynamics of stimulus movement have been proposed recently, but almost exclusively for nonlocomotor tasks by humans, such as oculomotor target tracking and posture control. These data suggest that such mechanisms might be common across taxa and behaviors. [ABSTRACT FROM AUTHOR]

Directional selectivity, in which neurons respond preferentially to one direction of movement ("preferred") over the opposite direction ("null"), is a critical computation that is found in the nervous systems of many animals. Here we show the first experimental evidence for a correlation between differences in short-term depression and direction-selective responses to moving objects. As predicted by quantitative models, the observed differences in the time courses of short-term depression at different locations within receptive fields were correlated with measures of direction selectivity in awake, behaving weakly electric fish (Apteronotus leptorhynchus). Because short-term depression is ubiquitous in the central nervous systems of vertebrate animals, it may be a common mechanism used for the generation of directional selectivity and other spatiotemporal computations. [ABSTRACT FROM AUTHOR]

The discrimination of the direction of movement of sensory images is critical to the control of many animal behaviors. We propose a parsimonious model of motion processing that generates direction selective responses using short-term synaptic depression and can reproduce salient features of direction selectivity found in a population of neurons in the midbrain of the weakly electric fish Eigenmannia virescens. The model achieves direction selectivity with an elementary Reichardt motion detector: information from spatially separated receptive fields converges onto a neuron via dynamically different pathways. In the model, these differences arise from convergence of information through distinct synapses that either exhibit or do not exhibit short-term synaptic depression-short-term depression produces phase-advances relative to nondepressing synapses. Short-term depression is modeled using two state-variables, a fast process with a time constant on the order of tens to hundreds of milliseconds, and a slow process with a time constant on the order of seconds to tens of seconds. These processes correspond to naturally occurring time constants observed at synapses that exhibit short-term depression. Inclusion of the fast process is sufficient for the generation of temporal disparities that are necessary for direction selectivity in the elementary Reichardt circuit. The addition of the slow process can enhance direction selectivity over time for stimuli that are sustained for periods of seconds or more. Transient (i.e., short-duration) stimuli do not evoke the slow process and therefore do not elicit enhanced direction selectivity. The addition of a sustained global, synchronous oscillation in the gamma frequency range can, however, drive the slow process and enhance direction selectivity to transient stimuli. This enhancement effect does not, however, occur for all combinations of model parameters. The ratio of depressing and nondepressing synapses determines the effects of the addition of the global synchronous oscillation on direction selectivity. These ingredients, short-term depression, spatial convergence, and gamma-band oscillations, are ubiquitous in sensory systems and may be used in Reichardt-style circuits for the generation and enhancement of a variety of biologically relevant spatiotemporal computations. [ABSTRACT FROM AUTHOR]

How do neural systems process sensory information to control locomotion? The weakly electric knifefish Eigenmannia, an ideal model for studying sensorimotor control, swims to stabilize the sensory image of a sinusoidally moving refuge. Tracking performance is best at stimulus frequencies less than ∼1 Hz. Kinematic analysis, which is widely used in the study of neural control of movement, predicts commensurately low-pass sensory processing for control. The inclusion of Newtonian mechanics in the analysis of the behavior, however, categorically shifts the prediction: this analysis predicts that sensory processing is high pass. The counterintuitive prediction that a low-pass behavior is controlled by a high-pass neural filter nevertheless matches previously reported but poorly understood high-pass filtering seen in electrosensory afferents and downstream neurons. Furthermore, a model incorporating the high-pass controller matches animal behavior, whereas the model with the low-pass controller does not and is unstable. Because locomotor mechanics are similar in a wide array of animals, these data suggest that such high-pass sensory filters may be a general mechanism used for task-level locomotion control. Furthermore, these data highlight the critical role of mechanical analyses in addition to widely used kinematic analyses in the study of neural control systems. [ABSTRACT FROM AUTHOR]

Presents a study which determined the mechanisms responsible for generating temporal filters in the electrosensory system of electric fish Eigenmannia. Evidence for temporal filters in Eigenmannia; Gain-control processes associated with negative feedback.

The article offers information on a study which examines the significance of receptor trafficking as a mechanism for the regulation of proteins present on the cellular membrane. According to the author, the number of proteins at the membrane surface is controlled by the rate of exocytosis. Moreover, it mentions that higher rate of exocytosis will increase the number of proteins at the surface.

Objective: Sensory and motor systems are linked: motor actions alter the information that animals receive from their sensory receptors, which in turn is used to control subsequent motor actions. In active sensing, animals execute ancillary motor movements to obtain and/or modulate sensory information. The neural mechanisms for the control of active sensing are not known. Our goal is to describe the neurophysiological interactions between the sensory and motor circuits in the CNS toward understanding the neural mechanisms of the active sensing. Methods: Weakly electric fishes such as Apteronotus lep-torhynchus robustly perform an image stabilization task in which animals track the movement of a refuge in a single linear dimension. During this behavior, these animals produce large fore-aft movements for active sensing that modulate and maintain a robust level of sensory slip, the main form of feedback used in the control of refuge tracking. We performed chronic tetrode recordings in midbrain circuits of (n=17) Apteronotus during their free refuge tracking behavior to reveal the sensorimotor activity related to the control of these active sensing movements. We implanted electrodes in the Torus semicircularis, a midbrain electrosensory area where direction-selective responses first emerge. Results: We found direction-selective neurons, which respond to a range of velocities for the sensory slip, the error between the refuge and fish movements. Our analysis revealed that these direction-selective neurons are also selective for ranges of acceleration of the sensory slip. Midbrain electrosensory neurons responded best to high-frequency features, behaving as a high-pass filter on the sensory slip. Conclusion: The behavioral studies suggest high-pass sensorimotor transformations in the CNS. The spatiotemporal filtering properties of the midbrain neurons we obtained matched the predictions of the behavioral experiments. These preliminary findings are a first step toward understanding neural mechanisms for control of active sensing in a freely behaving animal. [ABSTRACT FROM AUTHOR]

The authors comment on the recent developments related to research on the behaviour, modulation, evolution and neural mechanisms of behaviour in electric fish. They emphasize the value of weakly electric fish and its neuroethology in the study of neural mechanisms. They describe the electrogenesis of the gymnotiforms and the mormyriforms, the two major groups of weakly electric fishes. They explain how the study of weakly electric fish can aid in the research into the modulation of behaviour.

An abstract of the research paper "Coding Motion Direction by Action Potential Patterns," by Eric S. Fortune and colleagues, presented at the Twentieth Annual Computational Neuroscience Meeting, held in Stockholm, Sweden, from July 23-28, 2011.

An abstract of the article "Parallel coding of first and second order stimulus attributes," by Patrick McGillivray, Katrin Vonderschen, Eric S Fortune, Maurice J. Chacron is presented.

Regenerative processes enhance postsynaptic potential (PSP) amplitude and behaviorally relevant temporal filtering in more than one-third of electrosensory neurons in the torus semicircularis of Eigenmannia. Data from in vivo current-clamp intracellular recordings indicate that these "regenerative PSPs" can be divided in two groups based on their half-amplitude durations: constant duration (CD) and variable duration (VD) PSPs. CD PSPs have half-amplitude durations of between 20 and 60 ms that do not vary in relation to stimulus periodicity. In contrast, the half-amplitude durations of VD PSPs vary in relation to stimulus periodicity and range from approximately 10 to 500 ms. Injection of 0.1 nA sinusoidal current through the recording electrode demonstrated that CD PSPs and not VD PSPs can be elicited by voltage fluctuations alone. In addition, CD PSPs were blocked by intracellular application of either QX-314 or QX-222, whereas VD PSPs were not. These in vivo data suggest, therefore, that CD PSPs are mediated by voltage-dependent Na+ conductances. [ABSTRACT FROM AUTHOR]