The principles of classification and a classification of mammals. Bulletin of the AMNH ; v. 85

In mammals, environmental sounds stimulate the auditory receptor, the cochlea, via vibrations of the stapes, the innermost of the middle ear ossicles. These vibrations produce displacement waves that travel on the elongated and spirally wound basilar membrane (BM). As they travel, waves grow in amplitude, reaching a maximum and then dying out. The location of maximum BM motion is a function of stimulus frequency, with high-frequency waves being localized to the “base” of the cochlea (near the stapes) and low-frequency waves approaching the “apex” of the cochlea. Thus each cochlear site has a characteristic frequency (CF), to which it responds maximally. BM vibrations produce motion of hair cell stereocilia, which gates stereociliar transduction channels leading to the generation of hair cell receptor potentials and the excitation of afferent auditory nerve fibers. At the base of the cochlea, BM motion exhibits a CF-specific and level-dependent compressive nonlinearity such that responses to low-level, near-CF stimuli are sensitive and sharply frequency-tuned and responses to intense stimuli are insensitive and poorly tuned. The high sensitivity and sharp-frequency tuning, as well as compression and other nonlinearities (two-tone suppression and intermodulation distortion), are highly labile, indicating the presence in normal cochleae of a positive feedback from the organ of Corti, the “cochlear amplifier.” This mechanism involves forces generated by the outer hair cells and controlled, directly or indirectly, by their transduction currents. At the apex of the cochlea, nonlinearities appear to be less prominent than at the base, perhaps implying that the cochlear amplifier plays a lesser role in determining apical mechanical responses to sound. Whether at the base or the apex, the properties of BM vibration adequately account for most frequency-specific properties of the responses to sound of auditory nerve fibers.

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Mechanics of the Mammalian Cochlea

A litter of four cats, born and raised in a soundproofed chamber, was studied in an attempt to determine which, if any, features of the auditory‐nerve response from routinely available cats might be due to the chronic effects of noise exposure. Two features of routine‐normal response were especially suspect in this regard: (1) a ’’notch’’ in the distribution of single‐unit thresholds centered at characteristic frequencies (CF’s) near 3 kHz and (2) a compression of the distribution of rates of spontaneous discharge for units with CF above 10 kHz. A third feature of response in routine animals was the presence of a small number (roughly 10%) of units with virtually no spontaneous discharge and very high thresholds, sometimes 80 dB less sensitive than high‐spontaneous units of similar CF. In the data from chamber‐raised animals, the high‐spontaneous units showed exceptionally low thresholds at all CF regions, however, there were signs of the midfrequency notch in the threshold distribution of at least two of these animals. The compression of the spontaneous rate distribution was not seen in any of the three most sensitive animals. The data suggest that there is a significant amount of ’’normal pathology’’ in the high‐CF units from routine animals. Low‐spontaneous, high‐threshold units were present in all four chamber‐raised ears with the same characteristics as in routine animals (exceptionally narrow tuning curves and exceptionally low maximum discharge rates) and at roughly the same percentage of the unit sample. A class of units with medium spontaneous rates and intermediate thresholds could also be identified. The possible significance of a classification of auditory‐nerve units according to spontaneous rate is discussed.

/pdf/auditory-nerve-response-from-cats-raised-in-a-low-noise-50dpqc8rk7.pdf

Auditory-nerve response from cats raised in a low-noise chamber.

Nothing in biology makes sense except in the light of evolution, quipped Theodosius Dobzhansky. The theory of evolution argues that each biological species was not suddenly and independently created but that all life forms are interrelated by virtue of having descended from common ancestors through the accumulation of modifications. Indeed, nothing we know about living organisms would make any sense if they were not so interrelated. And the theory that biological species are descended from common ancestors provides an indispensable heuristic to understand why living organisms are what they are and do what they do.

Nothing in Biology Makes Sense Except in the Light of Evolution

Hearing sensitivity in mammals is enhanced by more than 40 dB (that is, 100-fold) by mechanical amplification thought to be generated by one class of cochlear sensory cells, the outer hair cells. In addition to the mechano-electrical transduction required for auditory sensation, mammalian outer hair cells also perform electromechanical transduction, whereby transmembrane voltage drives cellular length changes at audio frequencies in vitro. This electromotility is thought to arise through voltage-gated conformational changes in a membrane protein, and prestin has been proposed as this molecular motor. Here we show that targeted deletion of prestin in mice results in loss of outer hair cell electromotility in vitro and a 40-60 dB loss of cochlear sensitivity in vivo, without disruption of mechano-electrical transduction in outer hair cells. In heterozygotes, electromotility is halved and there is a twofold (about 6 dB) increase in cochlear thresholds. These results suggest that prestin is indeed the motor protein, that there is a simple and direct coupling between electromotility and cochlear amplification, and that there is no need to invoke additional active processes to explain cochlear sensitivity in the mammalian ear.

Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier.

The hearing organ of the inner ear was the last of the paired sense organs of amniotes to undergo formative evolution. As a mechanical sensory organ, the inner-ear hearing organ's function depends highly on its physical structure. Comparative studies suggest that the hearing organ of the earliest amniote vertebrates was small and simple, but possessed hair cells with a cochlear amplifier mechanism, electrical frequency tuning, and incipient micromechanical tuning. The separation of the different groups of amniotes from the stem reptiles occurred relatively early, with the ancestors of the mammals branching off first, approximately 320 million years ago. The evolution of the hearing organ in the three major lines of the descendents of the stem reptiles (e.g., mammals, birds-crocodiles, and lizards-snakes) thus occurred independently over long periods of time. Dramatic and parallel improvements in the middle ear initiated papillar elongation in all lineages, accompanied by increased numbers of sensory cells with enhanced micromechanical tuning and group-specific hair-cell specializations that resulted in unique morphological configurations. This review aims not only to compare structure and function across classification boundaries (the comparative approach), but also to assess how and to what extent fundamental mechanisms were influenced by selection pressures in times past (the phylogenetic viewpoint).

https://www.pnas.org/content/pnas/97/22/11736.full.pdf

Cochlear mechanisms from a phylogenetic viewpoint

1. Introduction.- 1.1 The Phylogeny of Reptiles and Birds.- 1.2 Systematics and the Inner Ear of Lizards.- 1.3 Cochlear Microphonics and the Inner Ear.- 2. Hair Cells and the Origin of the Hearing Inner Ear.- 2.1 Evolutionary Origin of the Inner Ear Sensory Epithelia.- 2.2 An Introduction to Hair Cells.- 2.2.1 The Hair Cell.- 2.2.2 Tectorial Membrane and Hair Cell Environment.- 2.2.3 Polarization of the Hair Cell.- 2.2.4 Hair Cell Innervation.- 2.3 Electroreceptors.- 2.4 Properties of Hair Cells of the Frog Sacculus.- 2.4.1 Resting Potential and Transduction Currents.- 2.4.2 An Electrical Resonance in Saccular Hair Cells.- 3. The Middle Ear.- 3.1 Origin of the Middle Ear.- 3.2 Pathways of Sound to the Inner Ear.- 3.3 General Functional Considerations.- 3.3.1 Factors Involved in Impedance Matching.- 3.3.2 Disadvantage of the Second-order Lever System.- 3.3.3 The Middle Ear of Modern Reptiles and Birds: Structure.- 3.3.4 The Middle Ear of Modern Reptiles and Birds: Function.- 3.3.4.1 The Amplifying Effect of the Middle Ear.- 3.3.4.2 Transfer Characteristics of Bird and Reptile Middle Ear.- 3.4 The Middle Ear as a Pressure-gradient Receiver.- 4. General Anatomical Considerations: Inner Ear and Basilar Papilla.- 4.1 Otic Labyrinth and Cochlear Duct.- 4.2 The Tectorial Membrane.- 4.3 The Basilar Papilla.- 4.3.1 The Primitive Basilar Papilla.- 4.3.2 The Evolution of the Basilar Papilla.- 4.3.3 The Variety and Evolution of the Lizard Papilla.- 4.3.4 Innervation Patterns of the Basilar Papilla.- 5. Some Techniques Used in Hearing Research.- 5.1 Obtaining Reptiles.- 5.2 Anaesthesia and Surgery.- 5.3 Acoustic Stimulation.- 5.4 Measuring the Motion of Middle- and Inner Ear Structures.- 5.5 Recording the Electrical Activity of the Ear.- 5.6 Marking of Hair Cells and Nerve Fibres.- 5.7 Measuring Otoacoustic Emissions.- 5.8 Anatomical Studies of the Papilla.- 6. Turtles and Snakes.- 6.1 The Hearing Organ of the Red-eared Turtle Pseudemys (Chrysemys) scripta.- 6.1.1 The Turtle as an Experimental Preparation.- 6.1.2 Anatomy of the Papilla Basilaris.- 6.1.3 Electrical Activity of Hair Cells.- 6.1.3.1 Tuning Properties of Hair Cells.- 6.1.3.2 Ionic Basis of Electrical Tuning.- 6.1.3.3 Efferent Effects on Hair Cells.- 6.1.4 Direct Stimulation of the Stereovillar Bundle.- 6.1.5 The Activity of Auditory-nerve Fibres.- 6.1.6 A Behavioural Audiogram for the Red-eared Turtle.- 6.2 The Hearing of Snakes.- 7. The Alligator Lizard and Granite Spiny Lizard.- 7.1 Anatomy of the Papilla Basilaris.- 7.1.1 The Papilla of the Alligator Lizard.- 7.1.2 The Papilla of the Granite Spiny Lizard.- 7.2 Recordings from Hair Cells.- 7.3 Activity of Primary Auditory-nerve Fibres.- 7.3.1 Auditory-nerve Fibres of the Alligator Lizard.- 7.3.2 Auditory-nerve Fibres of the Granite Spiny Lizard.- 7.4 Mechanics of the Basilar Papilla and Micromechanics of the Hair Cell Bundles.- 8. The European Lizards, Lacertidae: Podarcis sicula and Podarcis muralis.- 8.1 Anatomy of the Hearing Organ.- 8.2 Activity Patterns of Auditory-nerve Fibres.- 8.2.1 Spontaneous Activity.- 8.2.2 Activity in Response to Tones.- 9. The Monitor Lizard, Varanus bengalensis.- 9.1 Anatomy of the Basilar Papilla.- 9.2 Activity Patterns of Primary Auditory Fibres.- 10. The Hearing of Geckos.- 10.1 The Basilar Papilla of the Tokay Gecko, Gekko gecko.- 10.2 Activity of Afferent Auditory-nerve Fibres in Gekko.- 10.2.1 Spontaneous Activity.- 10.2.2 Responses to Tonal Stimulation.- 10.2.3 Responses to Species-specific Vocalizations.- 10.3 Temperature Effect on Tuning.- 11. The Bobtail Skink, Tiliqua rugosa.- 11.1 Anatomy of the Hearing Organ.- 11.2 Activity Patterns of Auditory-nerve Fibres.- 11.2.1 Tuning Properties.- 11.2.2 Tonotopic Organization of the Papilla.- 11.2.3 Discharge Patterns of Single Fibres.- 11.3 Basilar-membrane Mechanical Response and a Model of Frequency Tuning in Tiliqua.- 11.4 Seasonal Effects on Hearing.- 12. The Hearing of the Caiman, Caiman crocodilus.- 12.1 Anatomy of the Basilar Papilla.- 12.2 Mechanics of the Basilar Membrane.- 12.3 Otoacoustic Emissions from the Caiman Ear.- 12.4 Discharge Patterns of Primary Auditory-nerve Fibres.- 12.5 Effects of Temperature on Tuning.- 13. The Peripheral Hearing Organ of Birds.- 13.1 The Anatomy of the Cochlear Duct.- 13.1.1 The Sensory Hair Cells.- 13.1.2 Patterns in the Arrangement of Hair Cell Stereovillar Bundles.- 13.1.2.1 The Papilla of Starlings, Pigeons, and Chickens.- 13.1.2.2 The Papilla of the Barn Owl.- 13.1.2.3 Functional Implications of Variations in Papillar Anatomy.- 13.1.3 Innervation of Avian Hair Cells.- 13.2 Macromechanics of the Avian Cochlea.- 13.3 Otoacoustic Emissions from the Starling Cochlea.- 13.4 Activity of Auditory-nerve Fibres.- 13.4.1 Spontaneous Activity.- 13.4.2 Frequency Selectivity of Single Nerve Fibres.- 13.4.3 Tonotopicity and the Localization of Active Afferents.- 13.4.4 Ontogeny of the Tonotopic Organization.- 13.4.5 Discharge Patterns to Pure Tones.- 13.4.5.1 Firing Rates to Tonal Stimuli.- 13.4.5.2 Phase-locking to Tonal Stimuli.- 13.4.5.3 Primary and Two-tone Suppression.- 13.4.5.4 Temperature Effects.- 14. Overview and Outlook.- 14.1 The Middle Ear and the Hearing Range.- 14.2 The Hearing Range and Papillar Development.- 14.3 Patterns in Spontaneous Activity.- 14.4 The Functions of the Tectorial Membrane.- 14.5 Specialization of Hair Cell Populations.- 14.6 Hair Cell Types and Innervation in Lizards.- 14.7 Frequency Selectivity of Vertebrate Auditory Receptors.- 14.8 Tonotopic Organization and its Evolution in Lizards.- 14.9 Mechanisms of Frequency Selectivity.- 14.9.1 Electrical Tuning.- 14.9.2 Hair Cell Micromechanics.- 14.9.3 Interaction of Hair Cell Groups with the Tectorial Membrane.- 14.9.4 Interactions Between Hair Cells and Basilar Membrane.- 14.10 Below and Above 1 kHz.- References.

Peripheral Hearing Mechanisms in Reptiles and Birds

1 An Outline of the Evolution of Vertebrate HearingOrgans.- 2 Environmental Variables and the Fundamental Nature of Hearing.- 3 Evolution of Sensory Hair Cells.- 4 Parallel Evolution in Fish Hearing Organs.- 5 The Evolution of Single- and Multiple-Ossicle Ears in Fishes and Tetrapods.- 6 Evolution of the Amphibian Ear.- 7 The Lizard Basilar Papilla and Its Evolution.- 8 Hearing Organ Evolution and Specialization: Archosaurs.- 9 Hearing Organ Evolution and Specialization: Early and Later Mammals.- 10 The Evolution of Central Pathways and Their Neural Processing Patterns.- 11 Advances and Perspectives in the Study of the Evolution of the Vertebrate Auditory System.- Appendix: Useful Concepts from Circuit Theory.

Evolution of the Vertebrate Auditory System

The last two decades have produced a great deal of evidence that in the mammalian organ of Corti outer hair cells undergo active shape changes that are part of a “cochlear amplifier” mechanism that...

https://www.physiology.org/doi/pdf/10.1152/jn.2001.86.2.541

Geoffrey A. Manley

Papers

Cochlear mechanisms from a phylogenetic viewpoint

Peripheral Hearing Mechanisms in Reptiles and Birds

Evolution of the Vertebrate Auditory System

Evidence for an Active Process and a Cochlear Amplifier in Nonmammals

Phylogenetic development of the cochlea and its innervation.