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Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear.
Brain Behav Evol. 2018; 92(1-2):1-31.BB

Abstract

The ear of extant vertebrates reflects multiple independent evolutionary trajectories. Examples include the middle ear or the unique specializations of the mammalian cochlea. Another striking difference between vertebrate inner ears concerns the differences in the magnitude of the endolymphatic potential. This differs both between the vestibular and auditory part of the inner ear as well as between the auditory periphery in different vertebrates. Here we provide a comparison of the cellular and molecular mechanisms in different endorgans across vertebrates. We begin with the lateral line and vestibular systems, as they likely represent plesiomorphic conditions, then review the situation in different vertebrate auditory endorgans. All three systems harbor hair cells bathed in a high (K+) environment. Superficial lateral line neuromasts are bathed in an electrogenically maintained high (K+) microenvironment provided by the complex gelatinous cupula. This is associated with a positive endocupular potential. Whether this is a special or a universal feature of lateral line and possibly vestibular cupulae remains to be discovered. The vestibular system represents a closed system with an endolymph that is characterized by an enhanced (K+) relative to the perilymph. Yet only in land vertebrates does (K+) exceed (Na+). The endolymphatic potential ranges from +1 to +11 mV, albeit we note intriguing reports of substantially higher potentials of up to +70 mV in the cupula of ampullae of the semicircular canals. Similarly, in the auditory system, a high (K+) is observed. However, in contrast to the vestibular system, the positive endolymphatic potential varies more substantially between vertebrates, ranging from near zero mV to approximately +100 mV. The tissues generating endolymph in the inner ear show considerable differences in cell types and location. So-called dark cells and the possibly homologous ionocytes in fish appear to be the common elements, but there is always at least one additional cell type present. To inspire research in this field, we propose a classification for these cell types and discuss potential evolutionary relationships. Their molecular repertoire is largely unknown and provides further fertile ground for future investigation. Finally, we propose that the ultimate selective pressure for an increased endolymphatic potential, as observed in mammals and to a lesser extent in birds, is specifically to maintain the AC component of the hair-cell receptor potential at high frequencies. In summary, we identify intriguing questions for future directions of research into the molecular and cellular basis of the endolymph in the different compartments of the inner ear. The answers will provide important insights into evolutionary and developmental processes in a sensory organ essential to many species, including humans.

Authors+Show Affiliations

Cochlea and Auditory Brainstem Physiology, Cluster of Excellence "Hearing4All", School of Medicine and Health Sciences, Carl von Ossietzky University Oldenburg, Oldenburg, Germany. Research Center Neurosensory Science, Carl von Ossietzky University Oldenburg, Oldenburg, Germany.Neurogenetics Group, Cluster of Excellence "Hearing4All", School of Medicine and Health Sciences, Carl von Ossietzky University Oldenburg, Oldenburg, Germany.Sensory Neuroscience Research Group, School of Pharmacy and Biomolecular Sciences, University of Brighton, Brighton, United Kingdom.Research Center Neurosensory Science, Carl von Ossietzky University Oldenburg, Oldenburg, Germany, hans.g.nothwang@uni-oldenburg.de. Neurogenetics Group, Cluster of Excellence "Hearing4All", School of Medicine and Health Sciences, Carl von Ossietzky University Oldenburg, Oldenburg, Germany, hans.g.nothwang@uni-oldenburg.de.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Review

Language

eng

PubMed ID

30415265

Citation

Köppl, Christine, et al. "Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear." Brain, Behavior and Evolution, vol. 92, no. 1-2, 2018, pp. 1-31.
Köppl C, Wilms V, Russell IJ, et al. Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear. Brain Behav Evol. 2018;92(1-2):1-31.
Köppl, C., Wilms, V., Russell, I. J., & Nothwang, H. G. (2018). Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear. Brain, Behavior and Evolution, 92(1-2), 1-31. https://doi.org/10.1159/000494050
Köppl C, et al. Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear. Brain Behav Evol. 2018;92(1-2):1-31. PubMed PMID: 30415265.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear. AU - Köppl,Christine, AU - Wilms,Viviane, AU - Russell,Ian John, AU - Nothwang,Hans Gerd, Y1 - 2018/11/09/ PY - 2018/07/17/received PY - 2018/09/09/accepted PY - 2018/11/12/pubmed PY - 2019/7/3/medline PY - 2018/11/12/entrez KW - Cell type KW - Cupula KW - Evolutionary development KW - High-frequency hearing KW - Lateral line KW - Microenvironment KW - Transcription factor KW - Vestibular system SP - 1 EP - 31 JF - Brain, behavior and evolution JO - Brain Behav. Evol. VL - 92 IS - 1-2 N2 - The ear of extant vertebrates reflects multiple independent evolutionary trajectories. Examples include the middle ear or the unique specializations of the mammalian cochlea. Another striking difference between vertebrate inner ears concerns the differences in the magnitude of the endolymphatic potential. This differs both between the vestibular and auditory part of the inner ear as well as between the auditory periphery in different vertebrates. Here we provide a comparison of the cellular and molecular mechanisms in different endorgans across vertebrates. We begin with the lateral line and vestibular systems, as they likely represent plesiomorphic conditions, then review the situation in different vertebrate auditory endorgans. All three systems harbor hair cells bathed in a high (K+) environment. Superficial lateral line neuromasts are bathed in an electrogenically maintained high (K+) microenvironment provided by the complex gelatinous cupula. This is associated with a positive endocupular potential. Whether this is a special or a universal feature of lateral line and possibly vestibular cupulae remains to be discovered. The vestibular system represents a closed system with an endolymph that is characterized by an enhanced (K+) relative to the perilymph. Yet only in land vertebrates does (K+) exceed (Na+). The endolymphatic potential ranges from +1 to +11 mV, albeit we note intriguing reports of substantially higher potentials of up to +70 mV in the cupula of ampullae of the semicircular canals. Similarly, in the auditory system, a high (K+) is observed. However, in contrast to the vestibular system, the positive endolymphatic potential varies more substantially between vertebrates, ranging from near zero mV to approximately +100 mV. The tissues generating endolymph in the inner ear show considerable differences in cell types and location. So-called dark cells and the possibly homologous ionocytes in fish appear to be the common elements, but there is always at least one additional cell type present. To inspire research in this field, we propose a classification for these cell types and discuss potential evolutionary relationships. Their molecular repertoire is largely unknown and provides further fertile ground for future investigation. Finally, we propose that the ultimate selective pressure for an increased endolymphatic potential, as observed in mammals and to a lesser extent in birds, is specifically to maintain the AC component of the hair-cell receptor potential at high frequencies. In summary, we identify intriguing questions for future directions of research into the molecular and cellular basis of the endolymph in the different compartments of the inner ear. The answers will provide important insights into evolutionary and developmental processes in a sensory organ essential to many species, including humans. SN - 1421-9743 UR - https://www.unboundmedicine.com/medline/citation/30415265/Evolution_of_Endolymph_Secretion_and_Endolymphatic_Potential_Generation_in_the_Vertebrate_Inner_Ear_ L2 - https://www.karger.com?DOI=10.1159/000494050 DB - PRIME DP - Unbound Medicine ER -
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