Evolutionary trends in directional hearing
Section snippets
Tympanic hearing is a true evolutionary novelty
The emergence of thin flexible tympana would have greatly increased the frequency range and sensitivity of hearing in air [7]. Tympana are not primitive to tetrapods, but instead the fossil record shows that the bony elements that support the tympanum appeared independently in the anurans, turtles, lepidosaurs, archosaurs, and mammals sometime in the Triassic, or about 120 Mya after the emergence of tetrapods [6••, 8••]. Thus, sensitive high frequency hearing evolved multiple times, in parallel.
Selection for hearing must act upon an existing octaval framework
In all vertebrates, first order medullary nuclei receive octaval input and project to the sensory midbrain [11]. The eighth nerve is part of the octavolateralis system (octaval = ear with hair cells; lateralis = external lateral line with hair cells). Although neighbors, the eighth, lateral line and electrosensory cranial nerves are distinct, with the eighth nerve originating from an otic placode separate from the adjacent lateral line and electrosensory placodes [12]. Electroreception is an
Neural processing of sound source location
Next we will consider how the neural coding of sound source location might have emerged.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Conflict of interest statement
Nothing declared.
Acknowledgements
We gratefully acknowledge helpful insights from Drs. Shigeru Kuratani, Geoff Manley, Luis Puelles and Peggy Edds-Walton and assistance from G. Capshaw. This research was sponsored by National Institute on Deafness and Other Communications Disorders (NIDCD) grant DC-000436 (CEC) and by the Danish National Science Foundation [grant DFF1323-00132] (JC-D).
References (50)
Some aspects of the evolution of hearing in vertebrates
Nature
(1971)- et al.
What's a cerebellar circuit doing in the auditory system?
Trends Neurosci
(2004) - et al.
Acoustical coupling of lizard eardrums
JARO
(2008) - et al.
Analytical model of internally coupled ears
JASA
(2010) Evolutionary paths to mammalian cochleae
JARO
(2012)Central neural systems subserving a homoplasous periphery
Am Zool
(1984)- et al.
Sound localization strategies in three predators
Brain Behav Evol
(2015) - et al.
Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods
J Exp Biol
(2015) - et al.
Hearing in the African lungfish (Protopterus annectens): pre-adaptation to pressure hearing in tetrapods?
Biol Lett
(2011) - et al.
Better than fish on land? Hearing across metamorphosis in salamanders
Proc R Soc B
(2015)
Evolutionary biology: the origin of terrestrial hearing
Nature
Evolution of a sensory novelty: tympanic ears and the associated neural processing
Brain Res Bull
Gaining Ground: The Origin and Evolution of Tetrapods
Developmental genetic bases behind the independent origin of the tympanic membrane in mammals and diapsids
Nat Commun
Central Auditory Pathways in Anamniotic Vertebrates
Ontogeny and phylogeny: a re-evaluation of conceptual relationships and some applications
Brain Behav Evol
Electrosensory ampullary organs are derived from lateral line placodes in bony fishes
Nat Commun
Central projections of the lateral line and eighth nerves in the bowfin, Amia calva
J Comp Neurol
Dendritic arbors and central projections of physiologically characterized auditory fibers from the saccule of the toadfish, Opsanus tau
J Comp Neurol
What the toadfish ear tells the toadfish brain about sound
Adv Exp Med Biol
The evolution of central pathways and their neural processing patterns
The central auditory system of reptiles and birds
Morphological and physiological development of auditory synapses
Hearing Res
Differential roles for EphA and EphB signaling in segregation and patterning of central vestibulocochlear nerve projections
PLOS ONE
The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis
Front Neuroanat
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