Auditory evoked potentials of the plainfin midshipman fish (Porichthys notatus): Implications for directional hearing

Abstract

The plainfin midshipman (Porichthys notatus) is an acoustically communicative teleost fish. Here, we evaluated auditory evoked potentials (AEPs) in reproductive female midshipman exposed to tones at or near dominant frequencies of the male midshipman advertisement call. An initial series of experiments characterized AEPs at behaviorally relevant suprathreshold sound levels (130-140 dB SPL re. 1 µPa). AEPs decreased in magnitude with increasing stimulus frequency and featured a stereotyped component at twice the stimulus frequency. Recording electrode position was varied systematically and found to affect AEP magnitude and phase characteristics. Later experiments employed stimuli of a single frequency to evaluate contributions of the saccule to the AEP, with particular attention to the effects of sound source azimuth on AEP amplitude. Unilateral excision of saccular otoliths (sagittae) decreased AEP amplitude; unexpectedly, decreases differed for right versus left otolith excision. A final set of experiments manipulated the sound pressure-responsive swim bladder. Swim bladder excision further reduced the magnitude of AEP responses, effectively eliminating responses at the standard test intensity (130 dB SPL) in some animals. Higher-intensity stimulation yielded response minima at forward azimuths ipsilateral to the excised sagitta, but average cross-azimuth modulation generally remained slight. Collectively, the data underscore that electrode position is an essential variable to control in fish AEP studies and suggest that in female midshipman: (1) the saccule contributes to the AEP, but its directionality as indexed by the AEP is limited, (2) a left-right auditory asymmetry may exist and (3) the swim bladder provides gain in auditory sensitivity that may be important for advertisement call detection and phonotaxis.

Noise-induced damage in the zebrafish inner ear endorgans: evidence for higher acoustic sensitivity of saccular and lagenar hair cells

“…According to our results, the saccule was the most sensitive endorgan to noise exposure based on the higher saccular hair cell loss and synaptopathy observed. These findings agree with most literature on fish auditory systems that report saccule as the major auditory endorgan (Brown et al, 2019;Coffin et al, 2012;Ladich and Schulz-Mirbach, 2016), including in zebrafish (Brown et al, 2019;Coffin et al, 2012;Ladich and Schulz-Mirbach, 2016;Lu and DeSmidt, 2013;Smith et al, 2011). Fish species that have accessory hearing structures and improved auditory abilities, such as otophysans that include zebrafish, possess Weberian ossicles connecting the saccule to the swim bladder, which is typically correlated with higher auditory sensitivities and/or expanded hearing range (reviewed in Braun and Grande, 2008).…”

“…Since field potential recordings from the zebrafish endorgans would be very difficult to perform due to the difficult access to the inner ear compared to other fish models (eg. midshipman fish, toadfish, and gobies (Brown et al, 2019;Lu et al, 2010;Vasconcelos et al, 2015), the present work provides an essential confirmation of the major sensitivity of the saccule to acoustic stimuli in the adult zebrafish.…”

“…The sensory role of the inner ear endorgans can be vestibular and/or auditory, depending on the response frequencies and how the brain uses the information encoded in the VIIIth nerve afferents that project into the first order octaval nuclei in the brainstem (McCormick, 1999). The saccule has been described as the main auditory endorgan in teleost fishes (Brown et al, 2019;Coffin et al, 2012;Ladich and Schulz-Mirbach, 2016;Lu and DeSmidt, 2013;Smith et al, 2011), although the auditory sensitivity of utricle (Denton and Gray, 1979;Lu et al, 2004;Rogers and Sisneros, 2020) and lagena (Lu et al, 2003;Meyer et al, 2012;Sand, 1974;Vetter et al, 2019) has also been reported in a few species.…”

Finite element modelling of sound transmission in the Weberian apparatus of zebrafish ( Danio rerio )

“…The combination of high-resolution CT imaging and advanced biomechanics simulation tools has opened new avenues for realistically modelling the function of conductive hearing apparatus and investigating their mechanical behaviour, which is also the methodology basis of this study. Finite element methods have been extensively applied to study sound conduction of tympanic ears presented in tetrapods, with a particular focus on the human ear [45,53,54,[58][59][60][61][62][63]. Comparative studies on non-human vertebrates are still limited on cat [64], gerbil [65], chickens [66], mallard [67], whale [68] and mouse [69,70].…”

“…Finite element methods have been extensively applied to study sound conduction of tympanic ears presented in tetrapods, with a particular focus on the human ear [ 45 , 53 , 54 , 58 – 63 ]. Comparative studies on non-human vertebrates are still limited on cat [ 64 ], gerbil [ 65 ], chickens [ 66 ], mallard [ 67 ], whale [ 68 ] and mouse [ 69 , 70 ].…”