Evolutionary Trends in Directional Hearing

Overview

Journal Curr Opin Neurobiol

Specialties Biology
Neurology

Date 2016 Jul 25

PMID 27448850

Citations 11

Authors

Catherine E Carr

Jakob Christensen-Dalsgaard

Affiliations

Soon will be listed here.

Abstract

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.

Citing Articles

Revisiting the Chicken Auditory Brainstem Response: Frequency Specificity, Threshold Sensitivity, and Cross Species Comparison.

Ordiway G, McDonnell M, Sanchez J Neurosci Insights. 2024; 19:26331055241228308.

PMID: 38304551 PMC: 10832403. DOI: 10.1177/26331055241228308.

Hearing without a tympanic ear.

Capshaw G, Christensen-Dalsgaard J, Carr C J Exp Biol. 2022; 225(12).

PMID: 35724322 PMC: 9250799. DOI: 10.1242/jeb.244130.

The Hair Cell α9α10 Nicotinic Acetylcholine Receptor: Odd Cousin in an Old Family.

Lipovsek M, Marcovich I, Elgoyhen A Front Cell Neurosci. 2021; 15:785265.

PMID: 34867208 PMC: 8634148. DOI: 10.3389/fncel.2021.785265.

Bone conduction pathways confer directional cues to salamanders.

Capshaw G, Christensen-Dalsgaard J, Soares D, Carr C J Exp Biol. 2021; 224(20.

PMID: 34581406 PMC: 8601709. DOI: 10.1242/jeb.243325.

Neuronal sensitivity to the interaural time difference of the sound envelope in the mouse inferior colliculus.

Ono M, Bishop D, Oliver D Hear Res. 2019; 385:107844.

PMID: 31759235 PMC: 6933070. DOI: 10.1016/j.heares.2019.107844.

References

Marin F, Puelles L . Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci. 1995; 7(8):1714-38. DOI: 10.1111/j.1460-9568.1995.tb00693.x. View

Willaredt M, Schluter T, Nothwang H . The gene regulatory networks underlying formation of the auditory hindbrain. Cell Mol Life Sci. 2014; 72(3):519-535. PMC: 11113740. DOI: 10.1007/s00018-014-1759-0. View

Edds-Walton P, Fay R . Directional and frequency response characteristics in the descending octaval nucleus of the toadfish (Opsanus tau). J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2008; 194(12):1013-29. DOI: 10.1007/s00359-008-0373-8. View

Striedter G . Stepping into the same river twice: homologues as recurring attractors in epigenetic landscapes. Brain Behav Evol. 1998; 52(4-5):218-31. DOI: 10.1159/000006565. View

Nothwang H . Evolution of mammalian sound localization circuits: A developmental perspective. Prog Neurobiol. 2016; 141:1-24. DOI: 10.1016/j.pneurobio.2016.02.003. View

Clack J . Evolutionary biology: The origin of terrestrial hearing. Nature. 2015; 519(7542):168-9. DOI: 10.1038/519168a. View

Cambronero F, Puelles L . Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras. J Comp Neurol. 2000; 427(4):522-45. DOI: 10.1002/1096-9861(20001127)427:4<522::aid-cne3>3.0.co;2-y. View

Palanca-Castan N, Koppl C . In vivo Recordings from Low-Frequency Nucleus Laminaris in the Barn Owl. Brain Behav Evol. 2015; 85(4):271-86. DOI: 10.1159/000433513. View

Koppl C, Carr C . Maps of interaural time difference in the chicken's brainstem nucleus laminaris. Biol Cybern. 2008; 98(6):541-59. PMC: 3170859. DOI: 10.1007/s00422-008-0220-6. View

10.

McCormick C . Central projections of the lateral line and eighth nerves in the bowfin, Amia calva. J Comp Neurol. 1981; 197(1):1-15. DOI: 10.1002/cne.901970102. View

11.

Edds-Walton P, Fay R, Highstein S . Dendritic arbors and central projections of physiologically characterized auditory fibers from the saccule of the toadfish, Opsanus tau. J Comp Neurol. 1999; 411(2):212-38. View

12.

Palanca-Castan N, Koppl C . Change in the coding of interaural time difference along the tonotopic axis of the chicken nucleus laminaris. Front Neural Circuits. 2015; 9:43. PMC: 4542463. DOI: 10.3389/fncir.2015.00043. View

13.

Vossen C, Christensen-Dalsgaard J, van Hemmen J . Analytical model of internally coupled ears. J Acoust Soc Am. 2010; 128(2):909-18. DOI: 10.1121/1.3455853. View

14.

Grothe B, Pecka M . The natural history of sound localization in mammals--a story of neuronal inhibition. Front Neural Circuits. 2014; 8:116. PMC: 4181121. DOI: 10.3389/fncir.2014.00116. View

15.

Christensen-Dalsgaard J, Carr C . Evolution of a sensory novelty: tympanic ears and the associated neural processing. Brain Res Bull. 2008; 75(2-4):365-70. PMC: 3269633. DOI: 10.1016/j.brainresbull.2007.10.044. View

16.

Edds-Walton P . What the Toadfish Ear Tells the Toadfish Brain About Sound. Adv Exp Med Biol. 2015; 877:197-226. DOI: 10.1007/978-3-319-21059-9_10. View

17.

Wullimann M, Mueller T, Distel M, Babaryka A, Grothe B, Koster R . The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis. Front Neuroanat. 2011; 5:27. PMC: 3085262. DOI: 10.3389/fnana.2011.00027. View

18.

Bech Christensen C, Lauridsen H, Christensen-Dalsgaard J, Pedersen M, Madsen P . Better than fish on land? Hearing across metamorphosis in salamanders. Proc Biol Sci. 2015; 282(1802). PMC: 4344139. DOI: 10.1098/rspb.2014.1943. View

19.

Farago A, Awatramani R, Dymecki S . Assembly of the brainstem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps. Neuron. 2006; 50(2):205-18. DOI: 10.1016/j.neuron.2006.03.014. View

20.

Tang Y, Christensen-Dalsgaard J, Carr C . Organization of the auditory brainstem in a lizard, Gekko gecko. I. Auditory nerve, cochlear nuclei, and superior olivary nuclei. J Comp Neurol. 2011; 520(8):1784-99. PMC: 4300985. DOI: 10.1002/cne.23013. View