The Octavolateralis System and Mauthner Cell: Interactions and Questions

This paper is an overview of some of the major points to arise in the accompanying contributions of this special symposium issue. The symposium papers arose out of discussions among investigators interested in the inner ear and Mauthner cell, with the focus on hydrodynamic components that activate the Mauthner cell through the octavolateralis system. The intention of the symposium was to investigate the possibility of using our knowledge of the Mauthner system to help understand acoustic processing by the ear, and of using, our knowledge of fish hearing to better understand Mauthner cell function. This is the first attempt to take a broad look at both systems to see how they might function together. As such, these proceedings can serve as a mini-tutorial for investiaators interested in one system or the other. In this summary paper we also identify some of the major uncertainties in our understanding of the ear-Mauthner connection. These include questions about: (1) the identity of the acoustic stimuli that are neuroethologically relevant to the Mauthner system; (2) the relative importance of the various octavolateralis inputs (acoustic, vestibular, or lateral line); (3) the contribution of the different various acoustic endorgans to the Mauthner system; (4) whether the Mauthner system can distinguish sound source location; and (5) whether Mauthner neurobiology is compatible with the prevailing model (the phase model) for determining sound source location by fishes. We believe these issues provide potentially useful avenues of future investigation that should give important insights into both acoustic processing by fish and the function of the Mauthner system

Effects of low frequency acoustic pulses on startle behaviour and EOD activity in elephantnose fish (Gnathonemus petersii)

The sensory system initiating C-response and electric organ discharge (EOD) response in the hearing specialist elephantnose fish was studied in an experimental swing chamber set-up. The swing chamber is specially designed for producing controlled low frequency acoustic stimulus waveforms. The waveforms studied in the experiments were single cycle sinusoids of initial acoustic pressure and particle acceleration in the frequency range 10 Hz to 30 Hz, and mimicked key components in the acoustic signature of charging predatory fish attacks. The aim of the study was to reveal how initial acoustic pressure and particle acceleration trigger the inner ear sensory system in elephantnose fish to produce acoustic EOD- and C-responses. Acoustic startle behaviour was found to be optimally triggered by a combination of acoustic particle acceleration and compression, and very rarely by the same level of acoustic particle acceleration and rarefaction. Startle behaviours were highly directional, and this was ascribed to inner ear detection and coding of the direction of the initial particle acceleration. In the centre of the test chamber, acoustic startle behaviours were triggered by the particle acceleration component alone, but at significantly lower probability than when combined with compression. Startle behaviours observed in response to the low frequency stimuli greatly extended the known audible hearing range in elephantnose fish. Contrary to general opinion within the field of fish hearing, it was shown that acoustic pressure sensitivity is of behavioural relevance at very low sonic and infrasonic frequencies. The results of the study support the view that acute acoustic pressure sensitivity evolved independently several times in fish as adaptations to perform differentiated and more adaptable escapes from striking predatory attacks. EOD-responses were produced by the acoustic stimuli, and were significantly stronger to compression stimuli than to rarefaction stimuli. Why elephantnose fish emit a strong burst of EODs during acoustic startle behaviour is unclear, but may perhaps be as a distraction of electro-sensitive predators.Finn Jørgen Walvigs FoundationM-ECO

Monosynaptic targets of utricular afferents in the larval zebrafish

The larval zebrafish acquires a repertoire of vestibular-driven behaviors that aid survival early in development. These behaviors rely mostly on the utricular otolith, which senses inertial (tilt and translational) head movements. We previously characterized the known central brainstem targets of utricular afferents using serial-section electron microscopy of a larval zebrafish brain. Here we describe the rest of the central targets of utricular afferents, focusing on the neurons whose identities are less certain in our dataset. We find that central neurons with commissural projections have a wide range of predicted directional tuning, just as in other vertebrates. In addition, somata of central neurons with inferred responses to contralateral tilt are located more laterally than those with inferred responses to ipsilateral tilt. Many dorsally located central utricular neurons are unipolar, with an ipsilateral dendritic ramification and commissurally projecting axon emerging from a shared process. Ventrally located central utricular neurons tended to receive otolith afferent synaptic input at a shorter distance from the soma than in dorsally located neurons. Finally, we observe an unexpected synaptic target of utricular afferents: afferents from the medial (horizontal) semicircular canal. Collectively, these data provide a better picture of the gravity-sensing circuit. Furthermore, we suggest that vestibular circuits important for survival behaviors develop first, followed by the circuits that refine these behaviors

Structural Diversity in the Inner Ear of Teleost Fishes: Implications for Connections to the Mauthner Cell

A body of literature suggests that the Mauthner cell startle response can be elicited by stimulation of the ear. While we know that there are projections to the M-cell from the ear, the specific endorgan(s) of the ear projecting to the M-cell are not known. Moreover, there are many reasons to question whether there is one pattern of inner ear to M-cell connection or whether the endorgan(s) projection to the M-cell varies in species that have different hearing capabilities of hearing structures. In this paper, we briefly review the structure of fish ears, with an emphasis on structural regionalization within the ear. We also review the central projections of the ear, along with a discussion of the limited data on projections to the M-cell

The response of marine finfish and invertebrates to seismic survey noise

The oil and gas industry is of major economic importance to Australia. Offshore seismic surveys are an essential component of exploration for fossil fuel reserves. Offshore seismic surveys involve the use of arrays of air-guns that produce repetitive high energy, low frequency sound. There is increasing concern about the effect that the noise generated by a seismic survey has on the surrounding marine life. Various species of captive marine fish and one species of squid were exposed to the noise from a single Bolt PAR 600 B air-gun with a 20 cui firing chamber and a source level at 1 m of 203.6 dB re 1 μPa mean squared pressure. Ten trials were conducted in Jervoise Bay and two were carried out off the coast of Exmouth. A different noise regime was used in each trial, however most involved the use of approach-depart scenarios to simulate an actual seismic survey and a 10 second duty cycle. Noise levels received by the animals ranged between 128 - 192 dB re 1 μPa mean squared pressure. Behavioural observations of the fish and squid were made before, during and after air-gun noise exposure. The physiological stress response of the fish was monitored by measuring plasma cortisol and glucose levels before and after noise exposure. The sensory epithelium was removed from the ears of the fish prior to, immediately after and up to 86 days after air-gun noise exposure and examined using a scanning electron microscope. No statistically significant physiological stress response in fish was detected as a result of the air-gun noise exposure regimes used. Significant damage to the ciliary bundles of the sensory epithelium of the sacculus was observed in pink snapper (Pugrus auratus) that had been exposed to air-gun noise between 144 - 191 dB re 1 μPa for 1.71 hours. No regeneration of the hair bundles was observed 58 days after exposure to air-gun noise.However, evidence of regeneration was observed between 58 and 86 days after noise exposure. Behavioural observations suggested that as air-gun noise levels increase, fish respond by swimming faster, in tighter groups and towards the bottom of the water column. Significant increases in alarm responses were observed in fish and squid to air-gun noise exceeding 158 - 163 dB re 1μPa. An increasing proportion of alarm responses were also observed as the noise level increased. A decrease in the frequency of alarm responses for repeated exposures was observed in squid and some fish. The implications of these findings are discussed with comparisons of noise levels measured from an actual 2678 cui seismic survey air-gun array

Infrasound initiates directional fast-start escape responses in juvenile roach Rutilus rutilus

Acoustic stimuli within the sonic range are effective triggers of C-type escape behaviours in fish. We have previously shown that fish have an acute sensitivity to infrasound also, with acceleration thresholds in the range of 10(-5) m s(-2). In addition, infrasound at high intensities around 10(-2) m s(-2) elicits strong and sustained avoidance responses in several fish species. In the present study, the possible triggering of C-escapes by infrasonic single-cycle vibrations was examined in juvenile roach Rutilus rutilus. The fish were accelerated in a controlled and quantifiable manner using a swing system. The applied stimuli simulated essential components of the accelerations that a small fish would encounter in the hydrodynamic flow field produced by a predatory fish. Typical C- and S-type escape responses were induced by accelerations within the infrasonic range with a threshold of 0.023 m s(-2) for an initial acceleration at 6.7 Hz. Response trajectories were on average in the same direction as the initial acceleration. Unexpectedly, startle behaviours mainly occurred in the trailing half of the test chamber, in which the fish were subjected to linear acceleration in combination with compression, i.e. the expected stimuli produced by an approaching predator. Very few responses were observed in the leading half of the test chamber, where the fish were subjected to acceleration and rarefaction, i.e. the stimuli expected from a suction type of predator. We conclude that particle acceleration is essential for the directionality of the startle response to infrasound, and that the response is triggered by the synergistic effects of acceleration and compression

Animal escapology I: theoretical issues and emerging trends in escape trajectories

Escape responses are used by many animal species as their main defence against predator attacks. Escape success is determined by a number of variables; important are the directionality (the percentage of responses directed away from the threat) and the escape trajectories (ETs) measured relative to the threat. Although logic would suggest that animals should always turn away from a predator, work on various species shows that these away responses occur only approximately 50–90% of the time. A small proportion of towards responses may introduce some unpredictability and may be an adaptive feature of the escape system. Similar issues apply to ETs. Theoretically, an optimal ET can be modelled on the geometry of predator–prey encounters. However, unpredictability (and hence high variability) in trajectories may be necessary for preventing predators from learning a simple escape pattern. This review discusses the emerging trends in escape trajectories, as well as the modulating key factors, such as the surroundings and body design. The main ET patterns identified are: (1) high ET variability within a limited angular sector (mainly 90–180deg away from the threat; this variability is in some cases based on multiple peaks of ETs), (2) ETs that allow sensory tracking of the threat and (3) ETs towards a shelter. These characteristic features are observed across various taxa and, therefore, their expression may be mainly related to taxon-independent animal design features and to the environmental context in which prey live – for example whether the immediate surroundings of the prey provide potential refuges

Use of baited remote underwater video (BRUV) and motion analysis for studying the impacts of underwater noise upon free ranging fish and implications for marine energy management

© 2016 Elsevier Ltd Free-ranging individual fish were observed using a baited remote underwater video (BRUV) system during sound playback experiments. This paper reports on test trials exploring BRUV design parameters, image analysis and practical experimental designs. Three marine species were exposed to playback noise, provided as examples of behavioural responses to impulsive sound at 163–171 dB re 1 μPa (peak-to-peak SPL) and continuous sound of 142.7 dB re 1 μPa (RMS, SPL), exhibiting directional changes and accelerations. The methods described here indicate the efficacy of BRUV to examine behaviour of free-ranging species to noise playback, rather than using confinement. Given the increasing concern about the effects of water-borne noise, for example its inclusion within the EU Marine Strategy Framework Directive, and the lack of empirical evidence in setting thresholds, this paper discusses the use of BRUV, and short term behavioural changes, in supporting population level marine noise management

A review of the neural basis underlying the acoustic startle response with a focus on recent developments in mammals

The startle response consists of whole-body muscle contractions, eye-blink, accelerated heart rate, and freezing in response to a strong, sudden stimulus. It is evolutionarily preserved and can be observed in any animal that can perceive sensory signals, indicating the important protective function of startle. Startle response measurements and its alterations have become a valuable tool for exploring sensorimotor processes and sensory gating, especially in the context of pathologies of psychiatric disorders. The last reviews on the neural substrates underlying acoustic startle were published around 20 years ago. Advancements in methods and techniques have since allowed new insights into acoustic startle mechanisms. This review is focused on the neural circuitry that drives the primary acoustic startle response in mammals. However, there have also been very successful efforts to identify the acoustic startle pathway in other vertebrates and invertebrates in the past decades, so at the end we briefly summarize these studies and comment on the similarities and differences between species