Cochlear apical morphology in toothed whales: Using the pairing hair cell—Deiters' cell as a marker to detect lesions

Abstract

The apex or apical region of the cochlear spiral within the inner ear encodes for low‐frequency sounds. The disposition of sensory hair cells on the organ of Corti is largely variable in the apical region of mammals, and it does not necessarily follow the typical three‐row pattern of outer hair cells (OHCs). As most underwater noise sources contain low‐frequency components, we expect to find most lesions in the apical region of the cochlea of toothed whales, in cases of permanent noise‐induced hearing loss. To further understand how man‐made noise might affect cetacean hearing, there is a need to describe normal morphological features of the apex and document interspecific anatomic variations in cetaceans. However, distinguishing between apical normal variability and hair cell death is challenging. We describe anatomical features of the organ of Corti of the apex in 23 ears from five species of toothed whales (harbor porpoise Phocoena phocoena, spinner dolphin Stenella longirostris, pantropical spotted dolphin Stenella attenuata, pygmy sperm whale Kogia breviceps, and beluga whale Delphinapterus leucas) by scanning electron microscopy and immunofluorescence. Our results showed an initial region where the lowest frequencies are encoded with two or three rows of OHCs, followed by the typical configuration of three OHC rows and three rows of supporting Deiters' cells. Whenever two rows of OHCs were detected, there were usually only two corresponding rows of supporting Deiters' cells, suggesting that the number of rows of Deiters' cells is a good indicator to distinguish between normal and pathological features.

Evidence of Hearing Loss and Unrelated Toxoplasmosis in a Free-Ranging Harbour Porpoise (Phocoena phocoena)

“…Specifically, evaluation of the left cochlea by SEM showed scattered OHC loss from 525–815 µm and focally at 1.5 mm from the apex. The lack of OHCs (especially OHCs from the third row) can be considered part of the normal apical variability in harbour porpoise and other animals [ 10 ]. However, because the ratio of hair cells and supporting Deiters cells is 1:1 [ 10 ], there was strong evidence of scars as a result of OHC death by apoptosis (orange arrows in Figure 4 ) in this case, rather than artefact or normal anatomic variation.…”

“…The lack of OHCs (especially OHCs from the third row) can be considered part of the normal apical variability in harbour porpoise and other animals [ 10 ]. However, because the ratio of hair cells and supporting Deiters cells is 1:1 [ 10 ], there was strong evidence of scars as a result of OHC death by apoptosis (orange arrows in Figure 4 ) in this case, rather than artefact or normal anatomic variation. The focal mild haemorrhage observed in the vestibular scala of the lower basal turn was possibly an artefactual transfer of erythrocytes from around the vein towards the cochlear aqueduct that may have occurred during the dissection or critical point drying process.…”

“…The disposition of sensory and supporting cells in the apex of the cochlea (the tip of the spiral, where the lowest frequencies are encoded) is variable. However, a recent study has described the arrangement of sensory cells in the apex of the harbour porpoise [ 10 ], providing baseline information on the common pattern in these species.…”

Selective Inner Hair Cell Loss in a Neonate Harbor Seal (Phoca vitulina)

“…The skull was opened with a hand saw to extract the brain, and the occipital bone was removed with a chisel T-Shape (Virchow skull breaker) post-mortem from the occipitomastoid suture ( Figure 1 a). The ear bones (periotic and tympanic) were separated and extracted from the squamosal bone using a chisel T-shape ( Figure 1 b), and the inner ears were perfused perilymphatically with 2.5% glutaraldehyde in 0.1M cacodylate buffer ( Figure 1 c), changed the media into 0.1M cacodylate buffer the following day, and subsequently processed for ultrastructural evaluation, following a previously optimized protocol for marine mammals [ 10 , 20 , 21 , 22 ].…”

Systematic validation and assessment of immunohistochemical markers for central nervous system pathology in cetaceans, with emphasis on auditory pathways

“…This is particularly relevant for markers of noise exposure, since the auditory sense predominates cetacean perception [ 25 ]. In fact, while methods to investigate harmful effects of underwater acoustic sources already exist for the inner ear of cetaceans [ 3 , 26 ], they are limited by carcass decomposition (i.e. they can be applied only a few hours from the death of the animals) and they may not provide conclusive information on other changes, such as tinnitus and non-auditory CNS pathology.…”