Dennis M. Higgs

Ultrasound detection by clupeiform fishes.

It has previously been shown that at least one species of fish (the American shad) in the order clupeiforms (herrings, shads, and relatives) is able to detect sounds up to 180 kHz. However, it has not been clear whether other members of this order are also able to detect ultrasound. It is now demonstrated, using auditory brainstem response (ABR), that at least one additional species, the gulf menhaden (Brevoortia patronus), is able to detect ultrasound, while several other species including the bay anchovy (Anchoa mitchilli), scaled sardine (Harengula jaguana), and Spanish sardine (Sardinella aurita) only detect sounds to about 4 kHz. ABR is used to confirm ultrasonic hearing in the American shad. The results suggest that ultrasound detection may be limited to one subfamily of clupeiforms, the Alosinae. It is suggested that ultrasound detection involves the utricle of the inner ear and speculate as to why, despite having similar ear structures, only one group may detect ultrasound.

Age- and Size-Related Changes in the Inner Ear and Hearing Ability of the Adult Zebrafish (Danio rerio)

Fishes, unlike most other vertebrate groups, continue to add sensory hair cells to their ears for much of their lives. However, it is not clear whether the addition ever stops or how the addition of sensory cells impacts hearing ability. In this article, we tested both questions using the zebrafish, Danio rerio. Our results not only have important implications for understanding the consequences of adding sensory receptors, but these results for normal zebrafish also serve as valuable baseline information for future studies of select mutations on the ear and hearing of this species. Our results show that hair cell production continues in uncrowded zebrafish up to 10 months of age (about one-third of a normal life span), but despite this addition there is no change in hearing sensitivity or bandwidth. Therefore, hearing is not related to the number of sensory cells in the ear in juvenile and adult animals. We also show that despite no net addition of hair cells after about 10 months, hair cells are still being produced, but at a lower rate, presumably to replace cells that are dying. Moreover, crowding of zebrafish has a marked impact on the growth of the fish and on the addition of sensory cells to the ear. We also demonstrate that fish size, not age, is a better indicator of developmental state of zebrafish.

Development of form and function in peripheral auditory structures of the zebrafish (Danio rerio)

Investigations of the development of auditory form and function have, with a few exceptions, thus far been largely restricted to birds and mammals, making it difficult to postulate evolutionary hypotheses. Teleost fishes represent useful models for developmental investigations of the auditory system due to their often extensive period of posthatching development and the diversity of auditory specializations in this group. Using the auditory brainstem response and morphological techniques we investigated the development of auditory form and function in zebrafish (Danio rerio) ranging in size from 10 to 45 mm total length. We found no difference in auditory sensitivity, response latency, or response amplitude with development, but we did find an expansion of maximum detectable frequency from 200 Hz at 10 mm to 4000 Hz at 45 mm TL. The expansion of frequency range coincided with the development of Weberian ossicles in zebrafish, suggesting that changes in hearing ability in this species are driven more by development of auxiliary specializations than by the ear itself. We propose a model for the development of zebrafish hearing wherein the Weberian ossicles gradually increase the range of frequencies available to the inner ear, much as middle ear development increases frequency range in mammals.

Sciaenid inner ears: A study in diversity

Sciaenid fishes (Family Sciaenidae) could potentially serve as models for understanding the relationship between structure and function in the teleost auditory system, as they show a broad range of variation in not only the structure of the ear but also in the relationship between the ear and swim bladder. In this study, scanning electron microscopy (SEM) was used to investigate inner ear ultrastructure of the Atlantic croaker (Micropogonias undulatus), spotted seatrout (Cynoscion nebulosus), kingfish (Menticirrhusamericanus) and spot (Leiostomus xanthurus). These species reflect the diversity of otolith and swim bladder morphology in sciaenids. The distribution of different hair cell bundle types, as well as hair cell orientation patterns on the saccular and lagenar maculae of these fishes were similar to one another. The rostral ends of the saccular sensory epithelia (maculae) were highly expanded in a dorsal-ventral direction in the Atlantic croaker and spotted seatrout as compared to the kingfish and spot. Also, ciliary bundles of the saccular maculae contained more stereocilia in the Atlantic croaker and spotted seatrout as compared with kingfish and spot. The shapes of the lagenar maculae were similar in all four species. In the Atlantic croaker and spotted seatrout lagenar maculae, the number of stereocilia per bundle was greater than those for the kingfish and spot. Given that saccular macula shape and numbers of stereocilia per bundle correlate with swim bladder proximity to the ear in the studied species, it is possible that inner ear ultrastructure could be indicative of auditory ability in fishes.

Audition in sciaenid fishes with different swim bladder-inner ear configurations.

We investigated how morphological differences in the auditory periphery of teleost fishes may relate to hearing capabilities. Two species of western Atlantic sciaenids were examined: weakfish (Cynoscion regalis, Block and Schneider) and spot (Leiostomus xanthurus, Lacepede). These species differ in the anatomical relationship between the swim bladder and the inner ear. In weakfish, the swim bladder has a pair of anterior horns that terminate close to the ear, while there are no extensions of the swim bladder in spot. Thus, the swim bladder in spot terminates at a greater distance from the ear when compared to weakfish. With the use of the auditory brainstem response technique, Cynoscion regalis were found to detect frequencies up to 2000 Hz, while Leiostomus xanthurus detected up to 700 Hz. There were, however, no significant interspecific differences in auditory sensitivity for stimuli between 200 and 700 Hz. These data support the hypothesis that the swim bladder can potentially expand the frequency range of detection.

Amphibious auditory responses of the American alligator (Alligator mississipiensis)

Abstract. Animals that thrive both on land and underwater are faced with the task of interpreting stimuli in different media. This becomes a challenge to the sensory receptors in that stimuli (e.g., sound, motion) may convey the same type of information but are transmitted with different physical characteristics. We used auditory brainstem responses to examine hearing abilities of a species that makes full use of these two environments, the American alligator (Alligator mississipiensis). In water, alligators responded to tones from 100xa0Hz to 2,000xa0Hz, with peak sensitivity at 800xa0Hz. In air, they responded to tones from 100xa0Hz to 8,000xa0Hz, with peak sensitivity around 1,000xa0Hz. We also examined the contribution to hearing of an air bubble that becomes trapped in the middle ear as the animal submerges. This bubble has been previously implicated in underwater hearing. Our studies show that the trapped air bubble has no affect on auditory thresholds, suggesting the bubble is not an important adaptation for underwater hearing in this species.

Neuronal turnover in the Xenopus laevis olfactory epithelium during metamorphosis

Metamorphic changes in the amphibian olfactory system present many interesting questions concerning the competing possibilities of neuronal respecification versus replacement. For example, are olfactory neurons retained during this transition with their presumed sensitivity to waterborne versus airborne stimuli respecified, or are olfactory neurons completely replaced? We address this question using the African clawed frog (Xenopus laevis) as a model. The water‐sensing nose (principal cavity; PC) of larval X. laevis is respecified into an air‐sensing cavity in adults, with changes in odorant receptor gene expression, ultrastructure, and site of innervation of the receptor neurons. The vomeronasal organ (VNO) does not appear to change function, structure, or innervation during metamorphosis. We labeled PC and VNO olfactory receptor neurons with injections of retrogradely transported fluorescent microspheres into the main and accessory olfactory bulbs. Injections were performed in larvae, and animals were allowed to survive through metamorphosis. After metamorphosis, few labeled cells were observed in the PC, whereas the VNO and the olfactory bulbs remained heavily labeled. Animals that were killed before metamorphosis always had extensive label in the PC epithelium regardless of how long the beads were present. This suggests that changes in the PC olfactory epithelium that are seen during metamorphosis are due primarily to turnover of the neurons in this epithelium rather than to respecification of existing neurons. These results also are discussed in terms of natural turnover time of olfactory receptor neurons. J. Comp. Neurol. 433:124–130, 2001.

DEVELOPMENT OF THE FISH AUDITORY SYSTEM: HOW DO CHANGES IN AUDITORY STRUCTURE AFFECT FUNCTION?

Ladich, F. & Yan, H.Y. (1998) Correlation between auditory sensitivity and vocalization in anabantoid fishes. J. Comp. Physiol. A 182, 737-746. Myrberg, A.A. & Spires, J.Y. (1980) Hearing in damselfishes: an analysis of signal detection among closely related species. J. Comp. Physiol. 140, 135-144. Ryan, M.J. & Keddy-Hector, A. (1992) Directional patterns of female mate choice and the role of sensory biases. Am. Natur. 139, 4-35.

Ultrasound detection by clupeiform fishes

It has previously been shown that at least one species of fish (the American shad) in the order clupeiforms (herrings, shads, and relatives) is able to detect sounds up to 180 kHz. However, it has not been clear whether other members of this order are also able to detect ultrasound. It is now demonstrated, using auditory brainstem response (ABR), that at least one additional species, the gulf menhaden (Brevoortia patronus), is able to detect ultrasound, while several other species including the bay anchovy (Anchoa mitchilli), scaled sardine (Harengula jaguana), and Spanish sardine (Sardinella aurita) only detect sounds to about 4 kHz. ABR is used to confirm ultrasonic hearing in the American shad. The results suggest that ultrasound detection may be limited to one subfamily of clupeiforms, the Alosinae. It is suggested that ultrasound detection involves the utricle of the inner ear and speculate as to why, despite having similar ear structures, only one group may detect ultrasound.

The enigma of fish ear diversity

There are substantial interspecific differences in the gross anatomy of fish inner ears, including the relative size of the different end organs and the sizes and shapes of their otoliths and sensory epithelia. Differences also occur at finer structural levels and include the orientation patterns of the ciliary bundles on the sensory hair cells. There is also substantial structural variation along the lengths of a single sensory epithelium. This includes not only the mode of contact between the sensory epithelium and the otolith, but also the lengths of the ciliary bundles on the hair cells, and the ultrastructure of the hair cell bodies themselves. The functional significance of the interspecific differences in ear structure is far from being understood, but it may reflect the evolution of different ways to do the same basic kinds of peripheral signal processing, or different kinds of signal processing. We also do not understand the functional importance of the intraepithelial differences, although they ...