Binaural Hearing: Lessons from Evolution

Conference on Neural Dynamics and Computation

in honor of John Rinzel

NYU Courant Institute June 2009

Cen

ozoi

cM

esoz

oic

Pal

eoz

oic

Quaternary

Tertiary

Cretaceous

Jurassic

Triassic

Permian

Carboniferous

Devonian

1.8

65

146

208

250

290

360

410

Rhipidistia

Early amphibians

“Stem reptiles”

DinosauriaPtero-sauria

Plesiosauria

Ichthyo-sauria

Thecodontia

SphenodontidaeTestudinesSquamataAnuraUrodela

Gymno-phiona

AvesCrocodilia

Mammalia

Pelycosauria

Therapsida

Modified from Grothe, Nat. Rev. Neurosci, 2003

Sensitive, high-frequency hearing of airborne sound may be a recent event in vertebrate evolution

Tetrapod auditory systems evolved in parallel

Hearing of airborne sound evolved multiple times - in parallel

• Each groups should be regarded as an independent experiment in hearing

• Current theories suggest that there are major differences between directional hearing in bird and mammal brainstem

• Compare with circuits for directional hearing in lizards

• Identify computational principles underlying sound localization

A circuit for detection of interaural time differences (ITD)

• Delay line inputs synapse on coincidence detector neurons

• These neurons compute the new variable, ITD, and transform the time code into a place code

Jeffress model

NM neurons project bilaterally to NL to form maps of ITD CONTRA

IPSI

ITD detection circuits in the barn owl conform to the Jeffress model

NL act as coincidence detectors

Sound signals from left & right ears converge through the two prominent dendrites

From Macleod, 2007 From Ashida, 2007

Similar (not identical) circuits in mammals

• Neurons in MSO act as coincidence detectors• But do the

inputs form a map of ITD?• Currently

debated

Does ITD coding require a map?• Harper and

McAlpine (2004) proposed optimal coding strategy for ITD depends on head size.

• Test their predictions in the chicken

Good enough solutions ?

• Gerbils may have a population rate code rather than a map.

• birds a ‘labeled line’ population code

Diagrams from Grothe and Köppl

Can evolutionary history explain the differences?• How did ITD

circuits evolve?

• Compare with other birds and alligators

• Do ITD computations constrain map formation?

DinosauriaPtero-sauria

AvesCrocodilia

computational principles in the auditory system

• Computing source location is evolutionarily important

• Birds, crocodilians and mammals use parallel coding strategies

• Lizards have another solution

• sound location circuits highlight evolutionary constraints in circuit design and coding

Binaural Hearing: Lessons from Evolution

• And at the same time tomorrow…

• Stay tuned for Leo van Hemmen’s talk

• Theory of internally coupled ears – the ICE model: How lizards and birds provide us with a novel category of hearing

Thanks, John !