Here, we review fish rheotaxis (orientation to flow) with the goal of placing it within a larger behavioral and multisensory context. Rheotaxis is a flexible behavior that is used by fish in a ...variety of circumstances: to search for upstream sources of current-borne odors, to intercept invertebrate drift and, in general, to conserve energy while preventing downstream displacement. Sensory information available for rheotaxis includes water-motion cues to the lateral line and body-motion cues to visual, vestibular or tactile senses when fish are swept downstream. Although rheotaxis can be mediated by a single sense, each sense has its own limitations. For example, lateral line cues are limited by the spatial characteristics of flow, visual cues by water visibility, and vestibular and other body-motion cues by the ability of fish to withstand downstream displacement. The ability of multiple senses to compensate for any single-sense limitation enables rheotaxis to persist over a wide range of sensory and flow conditions. Here, we propose a mechanism of rheotaxis that can be activated in parallel by one or more senses; a major component of this mechanism is directional selectivity of central neurons to broad patterns of water and/or body motions. A review of central mechanisms for vertebrate orienting behaviors and optomotor reflexes reveals several motorsensory integration sites in the CNS that could be involved in rheotaxis. As such, rheotaxis provides an excellent opportunity for understanding the multisensory control of a simple vertebrate behavior and how a simple motor act is integrated with others to form complex behaviors.
This paper gives a brief synopsis of the research career of S.C. in fish bioacoustics with an emphasis on dipole near fields. The hydroacoustic nature of the dipole near field and the effective ...stimuli to lateral line and auditory systems combine to produce a multisensory, range-fractionated region that is critically important to many fish behaviors. The mottled sculpin and goldfish lateral lines encode the spatial complexities of the near field as spatial excitation patterns along the body surface to provide instantaneous snapshots of various source features such as distance, orientation, and direction of movement. In contrast, the pressure-sensitive channel of the goldfish auditory system the anterior swim bladder (SB)-saccule complex encodes the spatial complexities in a temporal fashion whenever the position or orientation of the source changes with respect to the anterior SB. A full appreciation for how these somatotopic and egocentric representations guide fish behavior requires an understanding of how multisensory information, including vision, is combined in sensorimotor regions of the brain to effect behavior. A brief overview of vertebrate brain organization indicates that behaviors directed to or away from hydroacoustic sources likely involve a variety of mechanisms, behavioral strategies, and brain regions.
Nearly all underwater vehicles and surface ships today use sonar and vision for imaging and navigation. However, sonar and vision systems face various limitations, e.g., sonar blind zones, dark or ...murky environments, etc. Evolved over millions of years, fish use the lateral line, a distributed linear array of flow sensing organs, for underwater hydrodynamic imaging and information extraction. We demonstrate here a proof-of-concept artificial lateral line system. It enables a distant touch hydrodynamic imaging capability to critically augment sonar and vision systems. We show that the artificial lateral line can successfully perform dipole source localization and hydrodynamic wake detection. The development of the artificial lateral line is aimed at fundamentally enhancing human ability to detect, navigate, and survive in the underwater environment.
Information contained in the spatial excitation pattern along arrayed sensors in the lateral line system of Lake Michigan mottled sculpin, as well as other surface-feeding fish and amphibians, is ...thought to play a fundamental role in guiding prey-orienting behaviors. However, the way in which prey location is encoded by the excitation pattern and used by the nervous system to direct orienting behaviors is largely unknown. In this study, we test the hypothesis that mottled sculpin use excitation peaks (local 'hot spots') to determine the somatotopic location of an artificial prey (vibrating sphere/dipole source) along the body surface. Dipole orientation (axis of sphere vibration re: long axis of the fish) is manipulated to produce excitatory peaks in different body locations without changing the actual sphere location. Our results show that orienting accuracy is largely independent of source orientation, but not source distance and that turning directions are not guided by local hot spots in the somatotopic activation pattern of the lateral line.
Hair cells of the lateral line system in fish may differ in their susceptibility to damage by aminoglycoside antibiotics. Gentamicin has been reported to damage hair cells within canal neuromasts, ...but not those within superficial neuromasts. This finding, based on SEM imaging, indicates a distinction in the physiology of hair cells between the two classes of neuromast. Studies concerned with the individual roles of canal and superficial neuromasts in behavior have taken advantage of this effect in an attempt to selectively disable canal neuromasts without affecting superficial neuromast function. Here we present an experimental test of the hypothesis that canal neuromasts are more vulnerable to gentamicin than superficial neuromasts. We measured the effect of gentamicin exposure on hair cells using vital stains (DASPEI and FM1-43) in the neuromasts of Mexican blind cave fish (
Astyanax
fasciatus) and zebrafish (
Danio
rerio). Contrary to the findings of prior studies that used SEM, gentamicin significantly reduced dye uptake by hair cells of both canal and superficial neuromasts in both species. Therefore, lateral line hair cells of both neuromast types are vulnerable to gentamicin ototoxicity. These findings argue for a re-evaluation of the results of studies that have used gentamicin to differentiate the roles of the two classes of neuromast in fish behavior.
Lake Michigan mottled sculpin, Cottus bairdi, exhibit a lateral-line mediated, unconditioned orienting response, which is part of the overall prey capture behavior of this species and can be ...triggered in visually deprived animals by both live (e.g. Daphnia magna) and artificial (e.g. chemically inert vibrating sphere) prey. However, the extent to which background water motions (e.g. currents) might mask the detection of biologically significant stimuli like these is almost entirely unknown, despite the fundamental nature and importance of this question. To examine this question, the orienting response of mottled sculpin was used to measure threshold sensitivity to a nearby artificial prey (a 50 Hz vibrating sphere) as a function of background noise level (unidirectional currents of different flow velocities). Because many fish show unconditioned rheotaxis to uniform currents, we also measured the fish's angular heading relative to the oncoming flow in the absence of the signal. Frequency distributions of fish headings revealed positive rheotaxis to flows as low as 4 cm s(-1) and an increasing degree of alignment with the oncoming flow as a function of increasing flow velocity. Sculpin positioned in the upstream direction were able to detect relatively weak signals (estimated to be approx. 0.001-0.0001 peak-peak cm s(-1) at the location of the fish) in the presence of strong background flows (2-8 cm s(-1)), and signal levels at threshold increased by less than twofold for a fourfold increase in flow velocity. These results are consistent with the idea that lateral line canals behave as high-pass filters to effectively reject low frequency noises such as those caused by slow d.c. currents.
Rheotaxis is a widespread behavior with many potential benefits for fish and other aquatic animals, yet the sensory basis of rheotaxis under different fluvial conditions is still poorly understood. ...Here, we examine the role that vision and the lateral line play in the rheotactic behavior of a stream-dwelling species (Mexican tetra, Astyanax mexicanus) under both rectilinear and turbulent flow conditions. Turbulence lowered the flow speed at which threshold levels of rheotactic performance were elicited, an effect that was independent of sensory condition. Compared to fish with access to visual information, fish without access exhibited cross-stream casting behaviors and a decrease in the accuracy with which they oriented upstream. Visual deprivation effects were independent of availability of lateral line information and whether flow was rectilinear or turbulent. Fish deprived of lateral line information exhibited no measureable deficits under any of the conditions of this study. This study indicates that rheotactic abilities persist in the absence of both vision and lateral line under both turbulent and non-turbulent conditions, but that turbulence enhances either the motivation or ability of fish to orient to slow currents.
Lake Michigan mottled sculpin, Cottus bairdi, exhibit a naturally occurring and unconditioned orienting response that can be triggered by both live prey and chemically inert vibrating spheres, even ...in blinded animals. CoCl(2)-induced reductions of the orienting response demonstrate that the lateral line is required for this behavior in the absence of non-mechanosensory cues (such as vision), but shed no light on the relative contributions of superficial and canal neuromasts to this behavior. To determine the relative roles of these two subsystems, we measured the frequency with which mottled sculpin oriented towards a small vibrating sphere before and after two treatments: (i) immersion of fish in a solution of gentamicin, an aminoglycoside antibiotic that damages hair cells in canal, but not superficial, neuromasts; and (ii) scraping the skin of the fish, which damages the superficial, but not the canal, neuromasts. To ensure that both superficial and canal neuromasts were adequately stimulated, we tested at different vibration frequencies (10 and 50 Hz) near or at the best frequency for each type of neuromast. At both test frequencies, response rates before treatment were greater than 70 % and were significantly greater than 'spontaneous' response frequencies measured in the absence of sphere vibration. Response rates fell to spontaneous levels after 1 day of gentamicin treatment and did not return to pre-treatment levels for 10-15 days. In contrast, response rates stayed approximately the same after superficial neuromasts had been damaged by skin abrasion. Scanning electron microscopy confirmed hair cell damage (loss of apical cilia) in canal, but not superficial, neuromasts of gentamicin-treated animals after as little as 24 h of treatment. The sensory epithelium of canal neuromasts gradually returned to normal, following a time course similar to behavioral loss and recovery of the orienting response, whereas that of superficial neuromasts appeared normal throughout the entire period. This study shows that the orienting response of the mottled sculpin is mediated by canal neuromasts.
When encountering a unidirectional flow, many fish exhibit an unconditioned orienting response known as rheotaxis. This multisensory behavior can reportedly involve visual, vestibular, tactile and ...lateral line cues. However, the precise circumstances under which different senses contribute are still unclear and there is considerable debate, in particular, about the contributions of the lateral line. In this study, we investigate the rheotactic behavior of blind cavefish under conditions of spatially non-uniform flow (a jet stream), which in theory, should promote reliance on lateral line cues. The behavior of individual lateral line enabled and disabled fish was videorecorded under IR light in a square arena that prevented streamwise biases and that contained a narrow jet stream in the center of the tank. Whereas the stream's peak velocity (8 cm s(-1)) declined very little in the streamwise direction, it declined steeply in the cross-stream direction (∼3-4.5 cm s(-1) cm(-1)). Lateral line enabled fish showed higher levels of orientation to the stream and its source (a 1-cm-wide nozzle) when in the central (jet stream) region of the tank compared with surrounding regions, whereas lateral line disabled fish showed random orientations in all regions of the tank. The results of this study indicate that the spatial characteristics of flow play a role in determining the sensory basis of rheotaxis.
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