Sheryl Coombs

The Enigmatic Lateral Line System

Hearing in its broadest sense is the detection, by specialized mechanoreceptors, of mechanical energy propagated through the environment. In terrestrial vertebrates, this typically means inner ear transduction of air pressure waves radiating out from a sound source, though the detection of substrate vibrations can also be considered as a form of hearing. In aquatic environments, the extended contribution of incompressible flow in the near field of the source adds additional complexities, and both incompressible flow and propagated pressure waves are detected by a range of specialized hair cell mechanosensory systems. Hair cells are generalized mechanical transducers that respond to mechanical deformation of the receptor hairs at their apical surface. One of the interesting stories of hearing in general, and in aquatic vertebrates in particular, is how the structures associated with hair cell organs play a major role in modifying or channeling the environmental stimulus onto the hair cell receptors. Hence the peripheral anatomy determines to a large degree what particular stimulus feature is being encoded at the level of the hair cell.

The Mechanosensory Lateral Line System of the Hypogean form of Astyanax Fasciatus

The mechanosensory lateral line is a distributed, hair-cell based system which detects the water flow regime at the surface of the fish. Superficial neuromasts densely scattered over the surface of some cave fish detect the pattern of flow over the surface of the body and are important in rheotactic behaviors and perhaps in the localization of small vibrating sources. Canal neuromasts are very likely also involved in the detection of small planktonic prey, but seem also to play an essential role in replacing vision as the major sense by which blind cave-fish perceive their surroundings. The flow-field that exists around a gliding fish is perturbed by objects in the immediate vicinity, these perturbations are detected by the lateral line system. In this way the fish can build up a ‘picture’ of its environment, a process that has been called active hydrodynamic imaging. None of the lateral line behaviors exhibited by blind cave fish are necessarily exclusive to these species, but there is some evidence that their lateral line capabilities are enhanced with respect to their sighted relatives.

Modeling and measuring lateral line excitation patterns to changing dipole source locations

In order to determine excitation patterns to the lateral line system from a nearby 50 Hz oscillating sphere, dipole flow field equations were used to model the spatial distribution of pressures along a linear array of lateral line canal pores. Modeled predictions were then compared to pressure distributions measured for the same dipole source with a miniature hydrophone placed in a small test tank used for neurophysiological experiments. Finally, neural responses from posterior lateral line nerve fibers in the goldfish were measured in the test tank to demonstrate that modeled and measured pressure gradient patterns were encoded by the lateral line periphery. Response patterns to a 50 Hz dipole source that slowly changed location along the length of the fish included (1) peaks and valleys in spike-rate responses corresponding to changes in pressure gradient amplitudes, (2) 180° phase-shifts corresponding to reversals in the direction of the pressure gradient and (3) distance-dependent changes in the locations of peaks, valleys and 180° phase-shifts. Modeled pressure gradient patterns also predict that the number of neural amplitude peaks and phase transitions will vary as a function of neuromast orientation and axis of source oscillation. The faithful way in which the lateral line periphery encodes pressure gradient patterns has implications for how source location and distance might be encoded by excitation patterns in the CNS. Phase-shift information may be important for (1) inhibitory/excitatory sculpting of receptive fields and (2) unambiguously encoding source distance so that increases in source distance are not confused with decreases in source amplitude.

Smart Skins: Information Processing by Lateral Line Flow Sensors

The information processing capabilities of the lateral line system and its potential utility in surveying foreign environments and providing sensory guidance to autonomous vehicles in dark or highly turbulent conditions is reviewed. The lateral line is a spatially-distributed system of directionally-sensitive sensors that respond to low-frequency water motions created by nearby moving sources, the animals own movements, the ambient motions of the surrounding water, and distortions in ambient or self-generated motions caused by the presence of stationary objects. While lateral line sensors on the skin surface appear to serve behaviors dependent on large-scale stimuli, such as upstream orientation to bulk water flow, other sensors enclosed in fluid-filled canals appear to subserve behaviors requiring information about fine spatial details, such as prey localization. Stimulation patterns along sensor arrays provide rich information about the location, distance and direction of moving sources. The lateral line system has also evolved several different mechanisms—static biomechanical filters at the periphery and dynamic neural filters in the central nervous system—for enhancing signal-to-noise ratios in different behavioral contexts, ranging from unexpected events of importance (e.g., an approaching predator or prey) to expected events of little relevance (e.g., the animals own repeated and regular breathing movements).

Behavioral and neurophysiological assessment of lateral line sensitivity in the mottled sculpin, Cottus bairdi.

Summary1.The unconditioned feeding response of the mottled sculpin, Cottus bairdi, was used to measure threshold sensitivity of the lateral line system to a vibrating sphere as a function of stimulus position (i.e. sphere near head, trunk or tail) and vibration frequency. In addition, extracellular recording techniques were used to measure threshold sensitivity curves for posterior lateral line nerve fibers for the same stimulus position used for measuring trunk sensitivity in behavioral measurements.2.For all stimulus positions, behaviorally-measured threshold sensitivity was relatively independent of vibration frequency from 10 to 100 Hz when defined in terms of water acceleration, rather than velocity or displacement. Best thresholds for stimuli placed 15 mm away from the head were around -75 dB re: 1 m/s2, approximately 20 dB less than that for stimuli placed at the same distance near the tail. Trunk sensitivity was intermediate.3.Physiologically-measured threshold sensitivity, in terms of acceleration, was also relatively independent of frequency from 10 to 100 Hz in most fibers. A smaller number of fibers showed a decline in acceleration sensitivity after 10–30 Hz, with the rate of decline being equivalent to equal velocity sensitivity. Best sensitivity of all fibers fell between -40 and -70 dB re: 1m/s2.4.These results indicate that (a) behavioral thresholds are based on acceleration-sensitive endorgans — most likely lateral line canal (rather than superficial) neuromasts, (b) behavioral performance can be accounted for on the basis of information from a single population of fibers, and (c) sensitivity varies along the fishs body in a manner that corresponds to the size and distribution of neuromasts.

Hearing differences among Hawaiian squirrelfish (family Holocentridae) related to differences in the peripheral auditory system

Summary1.Auditory sensitivity as a function of frequency has been behaviorally determined for two species of fish from the teleost family Holocentridae which is characterized by marked variation in peripheral auditory structures.2.Best sensitivity measured forMyripristis kuntee was -50 dB re: 1 dyne/cm2 for frequencies between 300 and 2,000 Hz, while best sensitivity measured forAdioryx xantherythrus was -28 dB at 500 Hz (Figs. 1 and 2).3.Both species can detect sounds at 100 Hz while the high frequency end of the auditory range extends up to 3,000 Hz forM. kuntee and to 800 Hz forA. xantherythrus (Figs. 1 and 2).4.It is hypothesized that these differences in auditory capabilities are related to differences in sound transmission characteristics of the peripheral auditory system.

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).

SUMMARY 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 fishs 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.

Neural mechanisms in sound detection and temporal summation.

The psychophysics and neurophysiology of sound detection in quiet and under noise masking were studied in goldfish. Psychophysical masking is a linear function of masker level. For long duration signals, signal-to-noise ratios (S/N) at threshold are 15.5, 19, and 22.5 dB for 200, 400 and 800 Hz signals, respectively, and is -5 dB for a noise signal. Threshold declines with signal duration to about 700 ms. The slopes of the masked temporal summation functions are about unity, indicating that energy is constant at threshold. In quiet however, the slopes are generally less than 0.5, indicating that shorter signals are detected at lower energy. Neural correlates of the masked S/Ns and the slopes of temporal summation functions were sought in the response patterns of single saccular neurons. Rate- and synchronization-intensity functions were obtained for tone and noise signals in quiet and in noise. S/Ns at behavioral threshold correspond closely to those required to raise spike rate just above that evoked by the masker alone, but are well above those required to cause clear synchronization. Therefore, sound detection is probably based on spike rate and not synchronization criteria. The equivalence of behavioral and neural thresholds indicates that the filters used in behavioral sound detection are simply the bandwidths of saccular fibers. A model outlined by Zwislocki which predicts the rate of temporal summation from the rate of growth of neural activity with intensity accounts quite well for the observed slopes of temporal summation functions both in quiet and in noise.

Dipole source localization by mottled sculpin. I. Approach strategies

Abstract Lake Michigan mottled sculpin respond to a chemically-inert vibrating sphere (a dipole source) with an initial orientation towards the source followed by a step-wise progression towards and final strike at the source. An analysis of videotape recordings of this behavior indicate that although pathways to the source varied, they tended to be influenced by the fishs position at signal onset. Fish heading toward the source at signal onset approached the source in an indirect fashion by either (a) keeping the source to one side in a smoothly arching path to the source or (b) alternating between keeping the source to the left and to the right. When the source was to the side of the fish at the time of stimulus onset, fish tended to approach the source in a more direct path. Most (79%) initial orienting responses placed the fish within 45° of the source, but response angles were not strongly correlated with initial source angle. Most (83%) unsuccessful strikes (misses) occurred when the source was directly in front of the fish (± 20°) and source angles associated with misses were significantly smaller than source angles associated with successful strikes. Approach strategies used by mottled sculpin in finding dipole sources appear to include (1) moving in a direction that increases the pressure difference along the head while keeping it consistently low (between 1 and 10 Pa) across the head, (2) narrowing the fish-to-source gap with each successive step in the pathway, (3) keeping the source lateralized (on average, 30° to one or the other side of the head) and (4) avoiding approach positions that are perpendicular to the flow line or that place the fish in the pressure null area of the dipole field. These results are consistent with the hypothesis that spatial excitation patterns along the lateral line system play a major role in encoding both source direction and distance.