Hormonal coordination of motor output and internal prediction of sensory consequences in an electric fish.

Steroid hormones remodel neural networks to induce seasonal or developmental changes in behavior. Hormonal changes in behavior likely require coordinated changes in sensorimotor integration. Here, we investigate hormonal effects on a predictive motor signal, termed corollary discharge, that modulates sensory processing in weakly electric mormyrid fish. In the electrosensory pathway mediating communication behavior, inhibition activated by a corollary discharge blocks sensory responses to self-generated electric pulses, allowing the downstream circuit to selectively analyze communication signals from nearby fish. These pulses are elongated by increasing testosterone levels in males during the breeding season. We induced electric-pulse elongation using testosterone treatment and found that the timing of electroreceptor responses to self-generated pulses was delayed as electric-pulse duration increased. Simultaneous recordings from an electrosensory nucleus and electromotor neurons revealed that the timing of corollary discharge inhibition was delayed and elongated by testosterone. Furthermore, this shift in the timing of corollary discharge inhibition was precisely matched to the shift in timing of receptor responses to self-generated pulses. We then asked whether the shift in inhibition timing was caused by direct action of testosterone on the corollary discharge circuit or by plasticity acting on the circuit in response to altered sensory feedback. We surgically silenced the electric organ of fish and found similar hormonal modulation of corollary discharge timing between intact and silent fish, suggesting that sensory feedback was not required for this shift. Our findings demonstrate that testosterone directly regulates motor output and internal prediction of the resulting sensory consequences in a coordinated manner.

Persistence of auditory modulation of wind-induced escape behavior in crickets.

Animals, including insects, change their innate escape behavior triggered by a specific threat stimulus depending on the environmental context to survive adaptively the predators' attack. This indicates that additional inputs from sensory organs of different modalities indicating surrounding conditions could affect the neuronal circuit responsible for the escape behavior. Field crickets, Gryllus bimaculatus, exhibit an oriented running or jumping escape in response to short air puff detected by the abdominal mechanosensory organ called cerci. Crickets also receive a high-frequency acoustic stimulus by their tympanal organs on their frontal legs, which suggests approaching bats as a predator. We have reported that the crickets modulate their wind-elicited escape running in the moving direction when they are exposed to an acoustic stimulus preceded by the air puff. However, it remains unclear how long the effects of auditory inputs indicating surrounding contexts last after the sound is terminated. In this study, we applied a short pulse (200 ms) of 15-kHz pure tone to the crickets in various intervals before the air-puff stimulus. The sound given 200 or 1000 ms before the air puff biased the wind-elicited escape running backward, like the previous studies using the longer and overlapped sound. But the sounds that started 2000 ms before and simultaneously with the air puff had little effect. In addition, the jumping probability was higher only when the delay of air puff to the sound was 1000 ms. These results suggest that the cricket could retain the auditory memory for at least one second and alter the motion choice and direction of the wind-elicited escape behavior.

Deep learning-assisted comparative analysis of animal trajectories with DeepHL.

A comparative analysis of animal behavior (e.g., male vs. female groups) has been widely used to elucidate behavior specific to one group since pre-Darwinian times. However, big data generated by new sensing technologies, e.g., GPS, makes it difficult for them to contrast group differences manually. This study introduces DeepHL, a deep learning-assisted platform for the comparative analysis of animal movement data, i.e., trajectories. This software uses a deep neural network based on an attention mechanism to automatically detect segments in trajectories that are characteristic of one group. It then highlights these segments in visualized trajectories, enabling biologists to focus on these segments, and helps them reveal the underlying meaning of the highlighted segments to facilitate formulating new hypotheses. We tested the platform on a variety of trajectories of worms, insects, mice, bears, and seabirds across a scale from millimeters to hundreds of kilometers, revealing new movement features of these animals.

A History of Corollary Discharge: Contributions of Mormyrid Weakly Electric Fish.

Corollary discharge is an important brain function that allows animals to distinguish external from self-generated signals, which is critical to sensorimotor coordination. Since discovery of the concept of corollary discharge in 1950, neuroscientists have sought to elucidate underlying neural circuits and mechanisms. Here, we review a history of neurophysiological studies on corollary discharge and highlight significant contributions from studies using African mormyrid weakly electric fish. Mormyrid fish generate brief electric pulses to communicate with other fish and to sense their surroundings. In addition, mormyrids can passively locate weak, external electric signals. These three behaviors are mediated by different corollary discharge functions including inhibition, enhancement, and predictive "negative image" generation. Owing to several experimental advantages of mormyrids, investigations of these mechanisms have led to important general principles that have proven applicable to a wide diversity of animal species.

Signal Diversification Is Associated with Corollary Discharge Evolution in Weakly Electric Fish.

Communication signal diversification is a driving force in the evolution of sensory and motor systems. However, little is known about the evolution of sensorimotor integration. Mormyrid fishes generate stereotyped electric pulses (electric organ discharge [EOD]) for communication and active sensing. The EOD has diversified extensively, especially in duration, which varies across species from 0.1 to >10 ms. In the electrosensory hindbrain, a corollary discharge that signals the timing of EOD production provides brief, precisely timed inhibition that effectively blocks responses to self-generated EODs. However, corollary discharge inhibition has only been studied in a few species, all with short-duration EODs. Here, we asked how corollary discharge inhibition has coevolved with the diversification of EOD duration. We addressed this question by comparing 7 mormyrid species (both sexes) having varied EOD duration. For each individual fish, we measured EOD duration and then measured corollary discharge inhibition by recording evoked potentials from midbrain electrosensory nuclei. We found that delays in corollary discharge inhibition onset were strongly correlated with EOD duration as well as delay to the first peak of the EOD. In addition, we showed that electrosensory receptors respond to self-generated EODs with spikes occurring in a narrow time window immediately following the first peak of the EOD. Direct comparison of time courses between the EOD and corollary discharge inhibition revealed that the inhibition overlaps the first peak of the EOD. Our results suggest that internal delays have shifted the timing of corollary discharge inhibition to optimally block responses to self-generated signals.SIGNIFICANCE STATEMENT Corollary discharges are internal copies of motor commands that are essential for brain function. For example, corollary discharge allows an animal to distinguish self-generated from external stimuli. Despite widespread diversity in behavior and its motor control, we know little about the evolution of corollary discharges. Mormyrid fishes generate stereotyped electric pulses used for communication and active sensing. In the electrosensory pathway that processes communication signals, a corollary discharge inhibits sensory responses to self-generated signals. We found that fish with long-duration pulses have delayed corollary discharge inhibition, and that this time-shifted corollary discharge optimally blocks electrosensory responses to the fish's own signal. Our study provides the first evidence for evolutionary change in sensorimotor integration related to diversification of communication signals.

Crickets alter wind-elicited escape strategies depending on acoustic context.

Acoustic signals trigger various behaviours in insects such as courtship or escape from predators. However, it remains unknown whether insects utilize acoustic signals to recognize environmental contexts. The cricket is a prominent model insect for neuroethological studies on acoustic behaviour because female crickets exhibit positive phonotaxis in response to male calling songs, and flying crickets display avoidance behaviour for high-frequency sounds such as echolocation call of bats. The carrier frequency of these sounds is a major factor in determining whether they initiate these acoustic behaviours. Here, we examined the impacts of different frequencies of tone sounds on cercal-mediated escape behaviour, using a 5-kHz tone corresponding to the calling song and a 15-kHz tone serving as a trigger of avoidance behaviours. Neither frequency elicited a response in the standing cricket by itself, but they had different impacts on walking responses to airflow stimuli. While the 15-kHz tone reduced response probability, extended moving distance, and enhanced turn-angle variability, the 5-kHz tone had no effect. Although both frequencies of tones facilitated walking backward, the 15-kHz tone had a larger effect than the 5-kHz tone. These frequency dependencies of behavioural modulation suggest that crickets can recognize acoustic contexts and alter their escape strategy accordingly.

Auditory modulation of wind-elicited walking behavior in the cricket Gryllus bimaculatus.

Animals flexibly change their locomotion triggered by an identical stimulus depending on the environmental context and behavioral state. This indicates that additional sensory inputs in different modality from the stimulus triggering the escape response affect the neuronal circuit governing that behavior. However, how the spatio-temporal relationships between these two stimuli effect a behavioral change remains unknown. We studied this question, using crickets, which respond to a short air-puff by oriented walking activity mediated by the cercal sensory system. In addition, an acoustic stimulus, such as conspecific 'song' received by the tympanal organ, elicits a distinct oriented locomotion termed phonotaxis. In this study, we examined the cross-modal effects on wind-elicited walking when an acoustic stimulus was preceded by an air-puff and tested whether the auditory modulation depends on the coincidence of the direction of both stimuli. A preceding 10 kHz pure tone biased the wind-elicited walking in a backward direction and elevated a threshold of the wind-elicited response, whereas other movement parameters, including turn angle, reaction time, walking speed and distance were unaffected. The auditory modulations, however, did not depend on the coincidence of the stimulus directions. A preceding sound consistently altered the wind-elicited walking direction and response probability throughout the experimental sessions, meaning that the auditory modulation did not result from previous experience or associative learning. These results suggest that the cricket nervous system is able to integrate auditory and air-puff stimuli, and modulate the wind-elicited escape behavior depending on the acoustic context.