A multisensory perspective on near-field detection and localization of hydroacoustic sourcesa).

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.

The career and research contributions of Richard R. Fay.

For over 50 years, Richard R. (Dick) Fay made major contributions to our understanding of vertebrate hearing. Much of Dick's work focused on hearing in fishes and, particularly, goldfish, as well as a few other species, in a substantial body of work on sound localization mechanisms. However, Dick's focus was always on using his studies to try and understand bigger issues of vertebrate hearing and its evolution. This article is slightly adapted from an article that Dick wrote in 2010 on the closure of the Parmly Hearing Institute at Loyola University Chicago. Except for small modifications and minor updates, the words and ideas herein are those of Dick.

Rheotaxis revisited: a multi-behavioral and multisensory perspective on how fish orient to flow.

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.

The influence of turbulence on the sensory basis of rheotaxis.

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.

The lateral line is necessary for blind cavefish rheotaxis in non-uniform flow.

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.

Sedentary behavior as a factor in determining lateral line contributions to rheotaxis.

Rheotaxis is a robust, multisensory behavior with many potential benefits for fish and other aquatic animals. Visual (optic flow) cues appear to be sufficient for rheotaxis, but other sensory cues can clearly compensate for the loss of vision. The role of various non-visual sensory systems, in particular the flow-sensing lateral line, is poorly understood, largely because of widely varying methods and sensory conditions for studying rheotaxis. Here, we examine how sedentary behavior under visually deprived conditions affects the relative importance of lateral line cues in two species: one that is normally sedentary (the three-lined corydoras, Corydoras trilineatus) and one that normally swims continuously along the substrate (the blind cavefish, Astyanax mexicanus). No effect of lateral line disruption on rheotactic performance was found in blind cavefish, which were significantly more mobile than three-lined corydoras. By contrast, rheotaxis was significantly impaired at low, but not high, flow speeds in lateral-line-disabled corydoras. In addition, lateral-line-enabled corydoras were characterized by decreased mobility and increased rheotactic performance relative to lateral-line-disabled fish. Taken together, these results suggest that sedentary behavior is an important factor in promoting reliance on lateral line cues.

Do blind cavefish have behavioral specializations for active flow-sensing?

Blind cavefish use a form of active sensing in which burst-coast swimming motions generate flow signals detected by the lateral line. To determine if blind cavefish have evolved behavioral specializations for active flow-sensing, including the ability to regulate flow signal production through lateral line feedback, the swimming kinematics of blind and sighted morphs of Astyanax were compared before and after 24 h of familiarization with a novel, dark environment and with and without lateral line functionality. Although both morphs showed little difference in the vast majority of kinematic parameters measured, blind morphs differed significantly from sighted morphs in having a much higher incidence of swim cycle sequences devoid of sharp turns. Both lateral line deprivation and familiarization with the arena led to significant declines in this number for blind, but not sighted morphs. These findings suggest that swimming kinematics are largely conserved, but that blind morphs have nevertheless evolved enhanced abilities to use lateral line feedback when linking swim cycles into continuous, straight trajectories for exploratory purposes. This behavioral specialization can best be understood in terms of the intermittent and short-range limitations of active flow-sensing and the challenges they pose for spatial orientation and navigation.

Dipole source encoding and tracking by the goldfish auditory system.

In goldfish and other otophysans, the Weberian ossicles mechanically link the saccule of the inner ear to the anterior swimbladder chamber (ASB). These structures are correlated with enhanced sound-pressure sensitivity and greater sensitivity at high frequencies (600-2000 Hz). However, surprisingly little is known about the potential impact of the ASB on other otolithic organs and about how auditory responses are modulated by discrete sources that change their location or orientation with respect to the ASB. In this study, saccular and lagenar nerve fiber responses and conditioned behaviors of goldfish were measured to a small, low-frequency (50 Hz) vibrating sphere (dipole) source as a function of its location along the body and its orientation with respect to the ASB. Conditioned behaviors and saccular nerve fiber activity exhibited response characteristics nearly identical to those measured from a hydrophone in the same relative position as the ASB. By contrast, response patterns from lagena fibers could not be predicted by pressure inputs to the ASB. Deflation of the ASB abolished the characteristic spatial response pattern of saccular but not lagena fibers. These results show that: (1) the lagena is not driven by ASB-mediated pressure inputs to the ear; (2) the ASB-saccule pathway dominates behavioral responsiveness, operating effectively at frequencies as low as 50 Hz; and (3) behavioral and neural (saccular) responses are strongly modulated by the position and orientation of the dipole with respect to the ASB.

Active wall following by Mexican blind cavefish (Astyanax mexicanus).

When introduced into a novel environment that limits or prevents vision, a variety of species including Mexican blind cavefish (Astyanax mexicanus) exhibit wall-following behaviors. It is often assumed that wall following serves an exploratory function, but this assertion remains untested against alternative artifactual explanations. Here, we test whether wall following by cavefish is a purposeful behavior in which fish actively maintain a close relationship with the wall, or an artifactual consequence of being enclosed in a small concave arena, in which fish turn slightly to avoid the wall whenever it impedes forward movement. Wall-following abilities of fish were tested in a large, goggle-shaped arena, where forward motion along the convex wall was unimpeded. In this circumstance, cavefish continued to follow the wall at frequencies significantly above chance levels. Lateral line inactivation significantly reduced the ability of fish to follow convex, but not concave or straight, walls. Wall-following abilities of normal fish decreased with decreasing radius of wall convex curvature. Our results demonstrate that cavefish actively follow walls of varying contours. Radius-of-curvature effects coupled with the difficulties posed by convex walls to lateral line-deprived fish suggest a partially complementary use of tactile and lateral line information to regulate distance from the wall.

Vibratory sources as compound stimuli for the octavolateralis systems: dissection of specific stimulation channels using multiple behavioral approaches.

Underwater vibratory sources simultaneously present acoustic and hydrodynamic disturbances. Because vibratory dipole sources are poor sonic projectors, most researchers have assumed that such sources are of greatest relevance to the lateral line system. Both hydroacoustic principles and empirical studies have shown that dipole sources are also a potent stimulus to the inner ear. Responses to vibratory sources in mottled sculpin (Cottus bairdi) were assessed using unconditioned orienting, differential and nondifferential conditioning. Orienting responses are dominated by lateral line inputs and eliminated by lateral line inactivation. Simple conditioning depends on inputs from other systems and was not affected by lateral line inactivation. Differential conditioning alters behavioral control, and sculpin could be conditioned to ignore substrate-borne vibrations and respond only to hydroacoustic stimulation of the ear. The lateral line and inner ear of mottled sculpin do not necessarily exhibit range fractionation, as both systems operate over a similar distance (within 1.5 body lengths) and respond to many of the same sources. Vibratory dipole sources generate compound stimuli that simultaneously activate multiple octavolateralis systems, and sculpin make use of the channels differentially under different behavioral tasks.

Gentamicin is ototoxic to all hair cells in the fish lateral line system.

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 (Astyanaxfasciatus) and zebrafish (Daniorerio). 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.

Using computational fluid dynamics to calculate the stimulus to the lateral line of a fish in still water.

This paper presents the first computational fluid dynamics (CFD) simulations of viscous flow due to a small sphere vibrating near a fish, a configuration that is frequently used for experiments on dipole source localization by the lateral line. Both two-dimensional (2-D) and three-dimensional (3-D) meshes were constructed, reproducing a previously published account of a mottled sculpin approaching an artificial prey. Both the fish-body geometry and the sphere vibration were explicitly included in the simulations. For comparison purposes, calculations using potential flow theory (PFT) of a 3-D dipole without a fish body being present were also performed. Comparisons between the 2-D and 3-D CFD simulations showed that the 2-D calculations did not accurately represent the 3-D flow and therefore did not produce realistic results. The 3-D CFD simulations showed that the presence of the fish body perturbed the dipole source pressure field near the fish body, an effect that was obviously absent in the PFT calculations of the dipole alone. In spite of this discrepancy, the pressure-gradient patterns to the lateral line system calculated from 3-D CFD simulations and PFT were similar. Conversely, the velocity field, which acted on the superficial neuromasts (SNs), was altered by the oscillatory boundary layer that formed at the fish's skin due to the flow produced by the vibrating sphere (accounted for in CFD but not PFT). An analytical solution of an oscillatory boundary layer above a flat plate, which was validated with CFD, was used to represent the flow near the fish's skin and to calculate the detection thresholds of the SNs in terms of flow velocity and strain rate. These calculations show that the boundary layer effects can be important, especially when the height of the cupula is less than the oscillatory boundary layer's Stokes viscous length scale.

Lateral line stimulation patterns and prey orienting behavior in the Lake Michigan mottled sculpin (Cottus bairdi).

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.

The function of wall-following behaviors in the Mexican blind cavefish and a sighted relative, the Mexican tetra (Astyanax).

Mexican blind cavefish exhibit an unconditioned wall-following behavior in response to novel environments. Similar behaviors have been observed in a wide variety of animals, but the biological significance and evolutionary history of this behavior are largely unknown. In this study, the behaviors of Mexican blind cavefish (Astyanax sp.) and sighted Mexican tetra (Astyanax mexicanus) were videotaped after fish were introduced into a novel environment under dark (infrared) or well-lit conditions. Under dark conditions, both sighted and blind morphs exhibited wall-following behaviors with subtle but significant differences. Blind morphs swam more nearly parallel to the wall, exhibited greater wall-following continuity and reached higher levels of sustained swimming speeds more quickly than sighted morphs. In contrast, sighted morphs in the light remained motionless near the wall for long periods of time or moved slowly around the center of the tank without entraining to the walls. These results are consistent with the idea that wall-following is a shared, primitive trait that serves an exploratory function under dark conditions to compensate for the absence of vision. This behavior has become more honed in blind morphs for exploratory purposes--in large part due to the enhanced, active-flow sensing abilities of the lateral line.

The hydrodynamic footprint of a benthic, sedentary fish in unidirectional flow.

Mottled sculpin (Cottus bairdi) are small, benthic fish that avoid being swept downstream by orienting their bodies upstream and extending their large pectoral fins laterally to generate negative lift. Digital particle image velocimetry was used to determine the effects of these behaviors on the spatial and temporal characteristics of the near-body flow field as a function of current velocity. Flow around the fish's head was typical for that around the leading end of a rigid body. Flow separated around the edges of pectoral fin, forming a wake similar to that observed for a flat plate perpendicular to the flow. A recirculation region formed behind the pectoral fin and extended caudally along the trunk to the approximate position of the caudal peduncle. In this region, the time-averaged velocity was approximately one order of magnitude lower than that in the freestream region and flow direction varied over time, resembling the periodic shedding of vortices from the edge of a flat plate. These results show that the mottled sculpin pectoral fin significantly alters the ambient flow noise in the vicinity of trunk lateral line sensors, while simultaneously creating a hydrodynamic footprint of the fish's presence that may be detected by the lateral line of nearby fish.

Distant touch hydrodynamic imaging with an artificial lateral line.

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.

Rheotaxis and prey detection in uniform currents by Lake Michigan mottled sculpin (Cottus bairdi).

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.

Modeling electrosensory and mechanosensory images during the predatory behavior of weakly electric fish.

Black ghost knifefish (Apteronotus albifrons) are nocturnal, weakly electric fish that feed on insect larvae and small crustaceans in the freshwater rivers of South America. In the absence of visual cues, prey detection and localization in this species is likely to rely on weak electrosensory and mechanosensory cues generated by the prey. In this paper, a modeling approach is used to estimate contributions to prey capture behavior from three octavolateralis modalities: the high- (tuberous) and low- (ampullary) frequency components of the electric sense and the high-frequency (canal neuromast) component of the lateral line mechanosensory system. For each of these modalities, the physical stimulus generated by the prey is approximated using a simple dipole model. Model parameters are constrained using previously published data as well as new empirical data on the electrical impedance characteristics of Daphnia magna. Models of electrosensory and mechanosensory stimuli are combined with actual prey strike trajectories from infrared video recordings to reconstruct spatial images of the prey along the sensory surface of the fish during the behavior. Modeling results suggest that all three modalities might contribute and that the relative contributions may change as a function of environmental conditions (e.g., water conductivity) and as a function of time over the course of the prey capture event.

Information-processing demands in electrosensory and mechanosensory lateral line systems.

The electrosensory and mechanosensory lateral line systems of fish exhibit many common features in their structural and functional organization, both at the sensory periphery as well as in central processing pathways. These two sensory systems also appear to play similar roles in many behavioral tasks such as prey capture, orientation with respect to external environmental cues, navigation in low-light conditions, and mediation of interactions with nearby animals. In this paper, we briefly review key morphological, physiological, and behavioral aspects of these two closely related sensory systems. We present arguments that the information processing demands associated with spatial processing are likely to be quite similar, due largely to the spatial organization of both systems and the predominantly dipolar nature of many electrosensory and mechanosensory stimulus fields. Demands associated with temporal processing may be quite different, however, due primarily to differences in the physical bases of electrosensory and mechanosensory stimuli (e.g. speed of transmission). With a better sense of the information processing requirements, we turn our attention to an analysis of the functional organization of the associated first-order sensory nuclei in the hindbrain, including the medial octavolateral nucleus (MON), dorsal octavolateral nucleus (DON), and electrosensory lateral line lobe (ELL). One common feature of these systems is a set of neural mechanisms for improving signal-to-noise ratios, including mechanisms for adaptive suppression of reafferent signals. This comparative analysis provides new insights into how the nervous system extracts biologically significant information from dipolar stimulus fields in order to solve a variety of behaviorally relevant problems faced by aquatic animals.