Binaural Hearing: Lessons from Evolution

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Binaural Hearing Lessons from Evolution

• Conference on Neural Dynamics and Computation
• in honor of John Rinzel
• NYU Courant Institute June 2009

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Tetrapod auditory systems evolved in parallel
Sphenodontidae
Mammalia
Gymno-phiona
Aves
Testudines
Squamata
Anura
Crocodilia
Urodela
Quaternary
1.8
Cenozoic
Tertiary
Plesiosauria
Ptero-sauria
Ichthyo-sauria
Dinosauria
65
Cretaceous
146
Mesozoic
Jurassic
208
Triassic
250
Thecodontia
Permian
Therapsida
Stem reptiles
290
Pelycosauria
Carboniferous
Paleozoic
Early amphibians
360
Modified from Grothe, Nat. Rev. Neurosci, 2003
Devonian
Rhipidistia
410
Sensitive, high-frequency hearing of airborne
sound may be a recent event in vertebrate
evolution
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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

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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
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ITD detection circuits in the barn owl conform to
the Jeffress model
IPSI
NM neurons project bilaterally to NL to form maps
of ITD
CONTRA
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NL act as coincidence detectors
Sound signals from left right ears converge
through the two prominent dendrites
From Macleod, 2007
From Ashida, 2007
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Similar (not identical) circuits in mammals

• Neurons in MSO act as coincidence detectors
• But do the inputs form a map of ITD?
• Currently debated

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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

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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
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Can evolutionary history explain the differences?
Crocodilia

• How did ITD circuits evolve?
• Compare with other birds and alligators
• Do ITD computations constrain map formation?

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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

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Binaural Hearing Lessons from Evolution

• And at the same time tomorrow
• Stay tuned for Leo van Hemmens talk
• Theory of internally coupled ears the ICE
  model How lizards and birds provide us with a
  novel category of hearing

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Thanks, John !