An official website of the United States government
The plainfin midshipman, Porichthys notatus, is a seasonally breeding vocal fish that relies on acoustic communication to mediate nocturnal reproductive behaviors. Reproductive females use their auditory senses to detect and localize “singing” males that produce multiharmonic advertisement (mate) calls during the breeding season. Previous work showed that the midshipman saccule, which is considered the primary end organ used for hearing in midshipman and most other fishes, exhibits reproductive state and hormone-dependent changes that enhance saccular auditory sensitivity. In contrast, the utricle was previously posited to serve primarily a vestibular function, but recent evidence in midshipman and related toadfish suggests that it may also serve an auditory function and aid in the detection of behaviorally relevant acoustic stimuli. Here, we characterized the auditory-evoked potentials recorded from utricular hair cells in reproductive and nonreproductive female midshipman in response to underwater sound to test the hypothesis that variation in reproductive state affects utricular auditory sensitivity. We show that utricular hair cells in reproductive females exhibit up to a sixfold increase in the utricular potential magnitude and have thresholds based on measures of particle acceleration (re: 1 ms −2 ) that are 7–10 dB lower than nonreproductive females across a broad range of frequencies, which include the dominant harmonics of male advertisement calls. This enhanced auditory sensitivity of the utricle likely plays an essential role in facilitating midshipman social and reproductive acoustic communication. NEW & NOTEWORTHY In many animals, vocal-acoustic communication is fundamental for facilitating social behaviors. For the vocal plainfin midshipman fish, the detection and localization of social acoustic signals are critical to the species’ reproductive success. Here, we show that the utricle, an inner ear end organ often thought to primarily serve a vestibular function, serves an auditory function that is seasonally plastic and modulated by the animal’s reproductive state effectively enhancing auditory sensitivity to courting male advertisement calls.
more »
« less
Response of toadfish ( Opsanus tau ) utricular afferents to multimodal inputs
The inner ear of teleost fishes is composed of three paired multimodal otolithic end organs (saccule, utricle, and lagena), which encode auditory and vestibular inputs via the deflection of hair cells contained within the sensory epithelia of each organ. However, it remains unclear how the multimodal otolithic end organs of the teleost inner ear simultaneously integrate vestibular and auditory inputs. Therefore, microwire electrodes were chronically implanted using a 3-D printed micromanipulator into the utricular nerve of oyster toadfish ( Opsanus tau) to determine how utricular afferents respond to conspecific mate vocalizations termed boatwhistles (180 Hz fundamental frequency) during movement. Utricular afferents were recorded while fish were passively moved using a sled system along an underwater track at variable speeds (velocity: 4.0–12.5 cm/s; acceleration: 0.2–2.6 cm/s 2 ) and while fish freely swam (velocity: 3.5–18.6 cm/s; acceleration: 0.8–29.8 cm/s 2 ). Afferent fiber activities (spikes/s) increased in response to the onset of passive and active movements; however, afferent fibers differentially adapted to sustained movements. In addition, utricular afferent fibers remained sensitive to playbacks of conspecific male boatwhistle vocalizations during both passive and active movements. Here, we demonstrate in alert toadfish that utricular afferents exhibit enhanced activity levels (spikes/s) in response to behaviorally relevant acoustic stimuli during swimming. NEW & NOTEWORTHY The inner ear of teleost fishes is composed of three paired multimodal otolithic end organs, which are sensitive to vestibular and auditory inputs. Previous studies investigating inner ear functions have primarily focused on the effects of unimodal stimuli; therefore, it remains unclear how otolithic end organs simultaneously encode multiple stimuli. Here, we show that utricular afferents remain sensitive to behaviorally relevant acoustic stimuli during swimming.
more »
« less
- Award ID(s):
- 1950380
- PAR ID:
- 10390374
- Date Published:
- Journal Name:
- Journal of Neurophysiology
- Volume:
- 128
- Issue:
- 2
- ISSN:
- 0022-3077
- Page Range / eLocation ID:
- 364 to 377
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract In seasonally breeding vertebrates, hormones coordinate changes in nervous system structure and function to facilitate reproductive readiness and success. Steroid hormones often exert their effects indirectly via regulation of neuromodulators, which in turn can coordinate the modulation of sensory input with appropriate motor output. Female plainfin midshipman fish (Porichthys notatus) undergo increased peripheral auditory sensitivity in time for the summer breeding season, improving their ability to detect mates, which is regulated by steroid hormones. Reproductive females also show differences in catecholaminergic innervation of auditory circuitry compared with winter, non-reproductive females as measured by tyrosine hydroxylase (TH), the rate-limiting enzyme in catecholaminergic synthesis. Importantly, catecholaminergic input to the inner ear from a dopaminergic-specific forebrain nucleus is decreased in the summer and dopamine inhibits the sensitivity of the inner ear, suggesting that gonadal steroids may alter auditory sensitivity by regulating dopamine innervation. In this study, we gonadectomized non-reproductive females, implanted them with estradiol (E2) or testosterone (T), and measured TH immunoreactive (TH-ir) fibers in auditory nuclei where catecholaminergic innervation was previously shown to be seasonally plastic. We found that treatment with T, but not E2, reduced TH-ir innervation in the auditory hindbrain. T-treatment also reduced TH-ir fibers in the forebrain dopaminergic cell group that projects to the inner ear, and likely to the auditory hindbrain. Higher T plasma in the treatment group was correlated with reduced-ir TH terminals in the inner ear. These T-treatment induced changes in TH-ir fibers mimic the seasonal downregulation of dopamine in the midshipman inner ear and provide evidence that steroid hormone regulation of peripheral auditory sensitivity is mediated, in part, by dopamine.more » « less
-
The biological inner ear, or cochlea, is an amazing sensor that performs auditory frequency analysis over an ultra-broadband frequency range of ~20 Hz to 20 kHz with exquisite sensitivity and high energy efficiency. Electronic cochlear models, which mimic the exponentially-tapered structure of the biological inner ear using transmission lines or filter cascades, have been shown to be fast and extremely efficient spectrum analyzers at both audio and radio frequencies (RF). Here we present improved output encoding methods for such cochlea-like analyzers. We have developed neuron-like asynchronous event-generation circuits to efficiently encode cochlear outputs, including ring-oscillator-based injection-locked frequency dividers (ILFDs) that accurately encode input frequencies and phase-sensitive detectors that encode both amplitude and phase information and thereby improve frequency resolution without reducing temporal resolution.more » « less
-
Teleost fishes have evolved a number of sound-producing mechanisms, including vibrations of the swim bladder. In addition to sound production, the swim bladder also aids in sound reception. While the production and reception of sound by the swim bladder has been described separately in fishes, the extent to which it operates for both in a single species is unknown. Here, using morphological, electrophysiological and modelling approaches, we show that the swim bladder of male plainfin midshipman fish (Porichthys notatus) exhibits reproductive state-dependent changes in morphology and function for sound production and reception. Non-reproductive males possess rostral ‘horn-like’ swim bladder extensions that enhance low-frequency (less than 800 Hz) sound pressure sensitivity by decreasing the distance between the swim bladder and inner ear, thus enabling pressure-induced swim bladder vibrations to be transduced to the inner ear. By contrast, reproductive males display enlarged swim bladder sonic muscles that enable the production of advertisement calls but also alter swim bladder morphology and increase the swim bladder to inner ear distance, effectively reducing sound pressure sensitivity. Taken together, we show that the swim bladder exhibits a seasonal functional plasticity that allows it to effectively mediate both the production and reception of sound in a vocal teleost fish.more » « less
-
Objective: To determine if a vestibular prosthesis could improve function in subjects with severe vestibular damage and could be used it as a scientific tool to investigate central vestibular processing. Background: Damage to the vestibular labyrinth is common and usually permanent. We therefore developed and tested a vestibular implant (VI) that is designed to mimic the information normally provided by the vestibular labyrinth to determine if we can reduce vestibular-mediated deficits and study temporal integration of sensory cues in the brain. Design/Methods: Monkeys had electrodes implanted in the semicircular canals of one ear and then severe bilateral vestibular damage was induced with aminoglycosides. Eye movements, perception, and balance were tested before and after vestibular damage and with the VI activated, which supplied head motion information to the brain via electrical stimulation delivered by the implanted electrodes. Humans also had electrode implantation (done in conjunction with a cochlear implant, CI) and they were tested on a temporal binding psychophysical task Results: Stimulation provided by VI in vestibulopathic monkeys improved their balance, perception of spatial orientation, and eye movement responses. Timing experiments in humans using CI and VI stimuli showed that unlike past experiments that used motion to generate the vestibular signal, CI and VI signals were received by the cerebral cortex with the same latency and were perceived as simultaneous, but this timing perception was highly sensitive to adaption. Conclusions: VI improves oculomotor, postural, and perceptual behavior in vestibulopathic monkeys and could prove to be an effective way to improve these functions in patients with permanent labyrinthine damage. Timing experiments show that when novel stimuli are used, the brain synthesizes them in accordance with their arrival at the cortex, but that experience can rapidly recalibrate this timing relationship, which may be why normal stimuli that are experienced habitually lack this characteristic.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1152/jn.00483.2021
