Elsevier

Current Opinion in Neurobiology

Volume 40, October 2016, Pages 111-117
Current Opinion in Neurobiology

Evolutionary trends in directional hearing

https://doi.org/10.1016/j.conb.2016.07.001Get rights and content

Highlights

  • Early tetrapods may have been pre-equipped for hearing in air.

  • Tympanic hearing is a true evolutionary novelty, and evolved multiple times among the tetrapods.

  • Selection for hearing likely acts upon an existing octaval framework like that in fishes.

  • ITD coding strategies vary among land vertebrates.

  • Differences may reflect both evolutionary history and environmental constraints.

Tympanic hearing is a true evolutionary novelty that arose in parallel within early tetrapods. We propose that in these tetrapods, selection for sound localization in air acted upon pre-existing directionally sensitive brainstem circuits, similar to those in fishes. Auditory circuits in birds and lizards resemble this ancestral, directionally sensitive framework. Despite this anatomically similarity, coding of sound source location differs between birds and lizards, although all show mechanisms for enhancing sound source directionality. Comparisons with mammals reveal similarly complex interactions between coding strategies and evolutionary history.

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)

  • J.A. Clack

    Evolutionary biology: the origin of terrestrial hearing

    Nature

    (2015)
  • J. Christensen-Dalsgaard et al.

    Evolution of a sensory novelty: tympanic ears and the associated neural processing

    Brain Res Bull

    (2008)
  • J.A. Clack

    Gaining Ground: The Origin and Evolution of Tetrapods

    (2012)
  • T. Kitazawa et al.

    Developmental genetic bases behind the independent origin of the tympanic membrane in mammals and diapsids

    Nat Commun

    (2015)
  • R.G. Northcutt et al.

    Central Auditory Pathways in Anamniotic Vertebrates

    (1980)
  • R.G. Northcutt

    Ontogeny and phylogeny: a re-evaluation of conceptual relationships and some applications

    Brain Behav Evol

    (1990)
  • M.S. Modrell et al.

    Electrosensory ampullary organs are derived from lateral line placodes in bony fishes

    Nat Commun

    (2011)
  • C.A. McCormick

    Central projections of the lateral line and eighth nerves in the bowfin, Amia calva

    J Comp Neurol

    (1981)
  • P.L. Edds-Walton et al.

    Dendritic arbors and central projections of physiologically characterized auditory fibers from the saccule of the toadfish, Opsanus tau

    J Comp Neurol

    (1999)
  • P.L. Edds-Walton

    What the toadfish ear tells the toadfish brain about sound

    Adv Exp Med Biol

    (2016)
  • B. Grothe et al.

    The evolution of central pathways and their neural processing patterns

  • C.E. Carr et al.

    The central auditory system of reptiles and birds

  • W.-M. Yu et al.

    Morphological and physiological development of auditory synapses

    Hearing Res

    (2014)
  • M.R. Allen-Sharpley et al.

    Differential roles for EphA and EphB signaling in segregation and patterning of central vestibulocochlear nerve projections

    PLOS ONE

    (2013)
  • M.F. Wullimann et al.

    The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis

    Front Neuroanat

    (2011)
  • Cited by (24)

    • 2.03 - How is the Vertebrate Auditory System Different From Other Senses?

      2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
    • 2.36 - Coding of Spatial Information

      2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
    • 2.19 - Evolution of Central Pathways

      2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
    • The Emergence of Mammals

      2020, Evolutionary Neuroscience
    • Neuronal sensitivity to the interaural time difference of the sound envelope in the mouse inferior colliculus

      2020, Hearing Research
      Citation Excerpt :

      However, the GABAergic neurons may contribute the sharpening of the ITD sensitivity of the postsynaptic neurons. In the medial superior olive (MSO) and nucleus laminaris (NL), avian analogue of MSO (Carr and Christensen-Dalsgaard, 2016; Grothe and Pecka, 2014; Lipovsek et al., 2018), ITD curves were suggested to be sharpen by inhibitory inputs (Brand et al., 2002; Funabiki et al., 1998; Nishino et al., 2008; Pecka et al., 2008; Yamada et al., 2013). Even though the inhibition from the GABAergic IC neuron may not convey ITD information, it might increase the conductance in the postsynaptic neurons (Funabiki et al., 1998) and sharpen the ITD tuning via ‘iceberg effect’ (Isaacson and Scanziani, 2011).

    • The Emergence of Mammals

      2016, Evolution of Nervous Systems: Second Edition
    View all citing articles on Scopus
    View full text