Olav Sand

Sound Detection Mechanisms and Capabilities of Teleost Fishes

This chapter, written from the perspective of four authors who have been studying fish bioacoustics for over 120 years (cumulative!), examines the major issues of the field. Each topic is put in some historical perspective, but the chapter emphasizes current thinking about acoustic communication, hearing (including bandwidth, sensitivity, detection of signals in noise, discrimination, and sound source localization), the functions of the ear (both auditory and vestibular, and including the role(s) of the otoliths and sensory hair cells) and their relationships to peripheral structures such as the swim bladder, and the interactions between the ear and the lateral line. Hearing in fishes is not only for acoustic communication and detection of sound-emitting predators and prey but can also play a major role in telling fishes about the acoustic scene at distances well beyond the range of vision. The chapter concludes with the personal views of the authors as to the major challenges and questions for future study. There are still many gaps in our knowledge of fish bioacoustics, including questions on ear function and the significance of interspecific differences in otolith size and shape and hair cell orientation, the role of the lateral line vis-a-vis the ear, the mechanisms of central processing of acoustic (and lateral line) signals, the mechanisms of sound source localization and whether fishes can determine source distance as well as direction, the evolution and functional significance of hearing specializations in taxonomically diverse fish species, and the origins of fish (and vertebrate) hearing and hearing organs.

Effects of different ionic environments on the mechano-sensitivity of lateral line organs in the mudpuppy

Summary1.The lateral line organ ofNecturus maculosus was stimulated with water vibrations, and the degree of synchronization between stimulus and afferent activity was related to the ionic composition of the external solution.2.The mechano-sensitivity was a function of the Ca++ concentration of the external medium (Fig. 2). The organs were insensitive to vibrations in Ca++ free solution (containing Ca-chelating agents) (Fig. 5), whereas the sensitivity leveled off at a maximum value for concentrations above about 1 mM Ca++. The effect of Sr++ was similar to Ca++ (Fig. 4). K+ and Na+ also enhanced the mechano-sensitivity, but the effect of these ions was much less than for Ca++ (Fig. 3).3.The mechano-sensitivity was suppressed by Mg++, Co++ and La+++ (Figs. 7, 8), the order of effectiveness being La+++≫ Co++> Mg++. The suppression decreased with increasing Ca++ concentration, suggesting that the effect of Ca++ is competitively blocked by these ions. The mechano-sensitivity was also suppressed by low pH (Fig. 9).4.The different ions tested in the present study affected the generation of hair cell receptor potentials, and it is suggested that the inward depolarizing receptor current of hair cells in mudpuppy lateral line organs is mainly carried by Ca++.

Low frequency hearing in cephalopods

SummaryClassical conditioning was employed to test the sensitivity of cephalopods to vibrations between 1 and 100 Hz generated in a standing wave acoustic tube. The animals were trained to associate sound stimuli with a weak electric shock, and the recorded conditioned responses were changes in breathing and jetting activity. Five specimens of Sepia officinalis were tested, and all responded to these low frequency sounds. The relevant stimulus parameter was particle motion rather than sound pressure. The threshold values (measured as particle acceleration) decreased towards lower frequencies in the tested range, reaching values below 4 × 10-3 m/s2. The thresholds in the most sensitive range may have been masked by the considerable background noise at the experimental site (Naples). Two individuals of Octopus vulgaris and one Loligo vulgaris were also tested, and showed a similar sensitivity to low frequency sound.

Directional hearing in the median vertical plane by the cod

SummaryThe ability of cod (Gadus morhua) to discriminate between sound sources in the median vertical plane was studied using a cardiac conditioning technique. Masked auditory thresholds were obtained by transmitting tone and noise from separate projectors. There was a significant decrease in masking as the angular separation between tone and noise sources increased, confirming that cod is able to perform an auditory discrimination based on directional cues (Fig. 2). The power of angular resolution was studied using a directional change of a pulsed tone as the conditioning stimulus. The limit for angular discrimination was close to 16°, as compared to 20° previously reported for the horizontal plane (Fig. 4). Humans are unable to discriminate between pure tones from different directions in the median vertical plane. This difference in auditory ability between fish and humans may be attributed to the difference in habitat; the fish living in a three dimensional medium while humans are restricted to a surface.

Behavioral Investigations on the Functions of the Lateral Line and Inner Ear in Predation

The lateral line, comprising the canal organs and free neuromasts, is generally regarded as a sensory system for the detection of local water currents (Hofer 1908; Dijkgraaf 1934) and surface waves (Schwartz 1965; Bleckmann et al., Chapter 25). However, whether the lateral line responds to low-frequency sound as well has long remained an issue of debate. Dijkgraaf (1963, Chapter 2) strongly argued against an acoustic function of the lateral line, citing a lack of compelling behavioral evidence. Sand (1981, 1984) explained that the operation of the lateral line in free-moving fish is physically restricted to the immediate vicinity of the source. Kalmijn (1988a, Chapter 9) subsequently focused attention on the function of the inner ear in detecting the local flow fields of moving objects at distances beyond the limited range of the lateral line. The lowfrequency nature of the two sensory systems is consistent with the results of earlier physiological studies (Suckling and Suckling 1950; Harris and van Bergeijk 1962; Enger 1966; Kalmijn 1988a).

Electrical and mechanical stimulation of hair cells in the mudpuppy

Summary1.The lateral line organ ofNecturus maculosus was stimulated with extracellular sine wave current, and the effect on the afferent activity was compared to the effect of mechanical vibration. Both mechanical and electrical stimulation caused phase locking between stimulus and afferent spikes (Figs. 2, 3).2.Intracellular recordings were made from the three main cell types of the neuromast: hair cells, supporting cells and afferent nerve terminals. Mechanical stimulation evoked receptor potentials of less than 1 mV in the hair cells. These potentials were synchronized with the stimulus (Fig. 6E), and mechanical stimulation caused a corresponding synchronization of action potentials in the afferent nerve terminals (Fig. 6A). The supporting cells were insensitive to vibrations (Fig. 6C).3.Intracellular injection of sine wave electrical current into hair cells caused synchrony between stimulus and afferent spikes (Fig. 6F), whereas even ten times more intense current was insufficient to cause such synchrony if the afferent nerve terminals were injected directly (Fig. 6B). Supporting cells were insensitive to electrical current stimulation (Fig. 6D).4.The effective intracellular current injections in the hair cells caused membrane potential changes which overlapped in magnitude with the naturally occurring receptor potentials. The conclusion is therefore that the mechanically evoked receptor potentials in hair cells have a direct effect on the transmitter release, and the potentials are not an epiphenomenon caused by the secretory activity of the hair cells.

Vasoactive intestinal peptide and peptide with N-terminal histidine and C-terminal isoleucine increase prolactin secretion in cultured rat pituitary cells (GE4C1) via a cAMP-dependent mechanism which involves transient elevation of intracellular Ca2+

Vasoactive intestinal peptide (VIP) and peptide (P) with N-terminal histidine and C-terminal isoleucine (PHI) stimulated prolactin (PRL) secretion from GH4C1 cells equipotent with ED50 values of 30-50 nM. In a parafusion system optimized to give high time resolution both VIP and PHI increased PRL secretion with a delay of about 60 s and subsequent to the activation of the adenylate cyclase. Thyroliberin (TRH) increased PRL secretion within 4 s. The dose-response curves for VIP- and PHI-stimulated cAMP accumulation were superimposable on those for PRL secretion. At submaximal concentrations the effects of VIP and PHI on both cAMP accumulation and PRL secretion were additive, whereas the effects were not additive at concentrations giving maximal effects. VIP and PHI increased [Ca2+]i measured by quin-2 in a different way than TRH, without inducing changes in the electrophysiological membrane properties of the GH4C1 cells. We conclude that both VIP and PHI stimulate PRL secretion via a cAMP-dependent process involving an increase in [Ca2+]i.

Avoidance responses to infrasound in downstream migrating European silver eels, (Anguilla anguilla)

In an attempt to develop an efficient acoustic fish fence, we have designed an infrasound source able to generate large nearfield particle acceleration. The source generates water movements by means of two symmetrical pistons in an air-filled cylinder with 21 cm bore. The pistons are driven by eccentric coupling to an electric motor, with 5 cm p.p. amplitude. The piston movements are 180° out of phase. The piston reaction forces are thus opposed, leading to vibration free operation. The submergible infrasound source is operated freely suspended in the water mass. The emitted sound frequency is 11.8 Hz. The particle acceleration is about 0.01 m s−2 at a distance of 3 m, corresponding to the threshold intensity for deterring effects of infrasound on Atlantic salmon smolts. The sound source was employed to test the effect of intense infrasound on migrating European silver eels. Fish confined in a tank displayed startle behaviour and prolonged stress reactions, telemetrically monitored as tachycardia, in response to intense infrasound. The field tests were carried out in the River Imsa. A trap that catches all the descending eels is installed near the river mouth. The trap was separated in four equal sections. During the periods with infrasound exposure, the proportion of silver eels entering the section closest to the sound source was reduced to 43% of the control value. In the section closest to the opposite river bank, infrasound increased the proportion of trapped eels to 144% of the control values. This shift of the migrating eels away from the infrasound source was highly significant.

Vibration measurements of the perch saccular otolith

Summary1.The vertical movement of different parts of the perch saccular otolith was measured with a laser vibrometer during horizontal vibration of the fish back and forth along its long axis. Data were obtained at four different frequencies within the audible range of the fish. Vibration at these frequencies caused very little vertical movement of the skull.2.No vertical oscillations of the otolith were detected at 20 Hz, whereas both ends of the otolith showed vertical vibrations at 40, 90 and 220 Hz. An area of minimum vertical movement appeared around the midpoint of the otolith at these frequencies, thus indicating the existence of a horizontal axis of rotation.3.It is argued that the stimulation technique is a reasonable approximation to underwater sound exposure. The measurements thus support the idea of a coarse, peripheral frequency analysis in fish based on a frequency dependent pattern of sound induced otolith movements.

Hearing in the eel (Anguilla anguilla)

SummaryThe auditory sensitivity in the European eel (Anguilla anguilla) was measured using an acoustic tube producing sound stimuli with different ratios between sound pressure and particle motion. The upper audible frequency limit in the eel was about 300 Hz. At low frequencies the relevant stimulus parameter was particle motion, excluding involvement of the swimbladder. At the higher frequencies within the audible range the swimbladder conveyed an auditory advantage for stimuli with a high ratio between pressure and particle motion. The eel has an extremely long distance between the swimbladder and the ear. An auditory function of the swimbladder in this species therefore indicates an efficient transmission channel for the reradiated swimbladder pulsations between the bladder and the ear, although specialized anatomical adaptations for this purpose are lacking.