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L14. Sound Localization 2

September 19, 2011

BioNB4240 C. D. Hopkins

Linear Summation Delay-line Coincidence Detector

delay

+ -

dthtfr )()()(Jeffress Model

neural delay, ΔT

coincidence detectors

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Jeffres’ Model (1948)

• Suppose Right & Left neural inputs from opposite sides converge....

• Delays, from neuronal conduction

• Output cells (A-E) fire only if there is coincident inputs from both R and L

• Delay-Line + coincidence detector produces a map of azimuth.

Barn Owl

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Barn Owls

Roger Payne established that barn owls hunt in total darkness by using passive listening (Payne, 1971)*. Later work by Masakazu Konishi established the owl as an experimental model system in Neuroethology.

* Payne, R. S. (1971) Acoustic location of prey by

Barn owls (Tyto alba)

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Owl can “localize” before leaving perch. Owl attack is precise within 2 degrees. Owl attacks sound source, not the mouse.

•Conclusion: good localization in both vertical (elevation) and horizontal (azimuth)

•How do they localize in the vertical?

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In barn owls, asymmetric ear placement converts IID into map of elevation

Right ear Left ear

0 0.5 1-1

-0.8

-0.6

-0.4

-0.2

0

0.2

0.4

0.6

0.8

1 y= x2

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Barn owl can locate speaker in two dimensions

Masakazu Konishi

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Head turning does not depend on feedback

• Short sounds: head turn begins after the sound.

• Magnitude of turn is correct for sounds of different directions.

• Accuracy is 1 to 2 degrees.

• Ballistic movement, no feedback needed.

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ILD Mapped

• Microphones in ear canals used to map difference in sound intensity

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Map of ITD

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Discovery: “A Neural Map of Auditory Space”

BioNB424

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Individual neurons in inferior colliculus are “space-tuned”. Their receptive fields are oval

shaped, tuned for sound direction.

Knudsen & Konishi (1978)

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Receptive field

Tuning to ITD

Tuning to ILD

Tuning is determined by two different sensory cues: ITD and ILD.

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A map of auditory space

Knudsen & Konishi (1978) 16

Single Cells in the IC

• space-tuned receptive fields

• arranged in a map of auditory space

• map is a “computational map” not a map of a sensory surface.

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Top Down Case in Point While I was waiting for the large anechoic room that was to be

assembled in my laboratory, I worked on the owl’s visual

Wulst with Jack Pettigrew. After one year of exciting research

with Jack, he asked me what I was going to do with the

auditory system. Since I was impressed by the selectivity of

visual neurons for space, I told him that I would like to map

the spatial receptive fields of auditory neurons. He

enthusiastically endorsed this idea and paid for the necessary

instruments to be built by the legendary designer and

machinist Herb Adams. The idea was to deliver sounds from

various directions to plot the distribution of neuronal responses

in space. About this time, Eric Knudsen asked me if he could

join me as a postdoc. Eric and I met in a café or hamburger

joint in Manhattan to discuss our project. When he asked me

what I was looking for, I answered "a map of auditory space,"

because the owl can rapidly pin point sound sources as if it

were using a look-up table. Eric said that he would expect a

map without any reason. We were naive and ignorant because

we did not know Arnold Starr’s review* in which he pointed

out that neither spatial receptive field or maps should exist in

the auditory system because space is not mapped in the inner

ear.

Mark Konishi

*Starr, A (1974) Fed Proc 1974 Aug;33(8):1911-4 Neurophysiological mechanisms of sound localization. 18

We did find neurons with spatial receptive fields first

in the forebrain auditory area. We could not, however,

recognize any map of auditory space. Eric suggested

that we go to the inferior colliculus. Since we could

not afford to kill an owl to make a brain atlas, we used

the head of a frozen owl. We cut it with a band saw

and look at unstained sections to determine the

coordinates of the inferior colliculus. In the first

multiunit recording, we saw a cluster of neurons

responding only to sound coming from a particular

direction. As I was leaving for somewhere, Eric

continued to record further. He later reported to me

that the preferred sound direction changed

systematically as he moved the electrode. We worked

very hard for about three months to find a map of

auditory space. Eric and I celebrated this occasion

with a bottle of champagne. - Mark Konishi

ISN Newsletter March 1999

http://www.neurobio.arizona.edu/isn/Newsletters/isn.n

ews.mar99.sec2.html#2

Eric Knudsen Roger( )

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Behavioral Test of ILD

• Trained owls

• Right ear plugged: owl turns down

• Left ear plugged, turns up

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Behavioral Test of ITD

• Owl presented with an artificial ITD from two earphones.

• Owl turns head after training to locate sounds at different azimuths

• Main cue: ongoing disparity of sound times (ITD)

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ITD Test • Behavioral test, trained owl.

• ITD manipulated with stereo headphones.

• Owl turns toward time-advanced sound.

• 10 microsec sensitivity.

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Hypothesis

• Vertical axis coded by IID

• Horizontal axis coded by ITD

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Time pathway in

the owl (blue)

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Cells in nucleus magnocellularis project to nucleus laminaris both ipsilaterally and contralerally. Ipsilateral axons enter dorsally; contralateral axons enter ventrally.

NL: azimuth maps onto depth in nucleus

NL analogous function to MSO in mammal

Carr, CE & Konishi, M 1988

1 mm

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C. Carr and M. Konishi find cells in nucleus magnocellularis that could generate a map of azimuth

NL: nucleus laminaris

NM: nucleus magnocellularis

Carr, CE & Konishi, M 1990

1 mm

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C. Carr and M. Konishi find cells in nucleus magnocellularis that could generate a map of azimuth

NL: nucleus laminaris

NM: nucleus magnocellularis

Carr, CE & Konishi, M 1990

1 mm

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Sullivan, W. E. and Konishi, M. find neural map of ITD in owl

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Konishi, 2006

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Map of Interaural Level Differences?

VLVp (nucleus Ventralis Lemnisci Lateralis pars posterior)

Takahashi, Barbarini, and Keller (1995) J. Comp. Neurol. 358:294 30

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31 Injections of tracer in the Right VLVp reveals terminals in the left dorsal VLVp

VLVp VLVp injection site

32 Injections of tracer in the Right VLVp reveals terminals in the left dorsal VLVp

Takahashi, T., C. L. Barberini, et al. (1995). "An anatomical substrate for the inhibitory gradient in the VLVp of the Owl " Journal of Comparative Neurology 359: 294-304.

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Time and Amplitude Pathways

Converge in the IC

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The two cochlear nuclei specialized for either time encoding or ampltiude encoding

• N. magnocellularis: – TIME PATHWAY

– thick axons; heavy myelin

– endbulb of Held

– adendritic cell

• N. anguilaris – AMPLITUDE PATHWAY

– small boutons

– diffuse arbor

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Vision guides plasticity

stimulus

stimulus

E. Knudsen, 1999

now owl responds normally to sound,

but makes 23 deg error to visual stim

After 42 days, the response to sound is also displaced

Sound Loclization_scenes.swf Sound Loclization_scenes.swf

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Q? How does the ITD map get

calibrated in development?

PNAS (1984)

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Head size is changing

PNAS (1984) 38

The Auditory Map is Plastic

1. Earplugs cause localization errors toward plugged ear.

2. These errors are temporary: after 2-3 weeks with earplugs, owls learn correct sound location.

3. After removal of ear plugs, owls again make errors.

4. These post-removal errors are also reversible (in young owls)

5. However, adults do not compensate for ear plugs.

Knudsen (1983)

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Vision is important in re-adjusting the

auditory map

• Errors corrected after ear plug removal (A, B)

• No correction if blinders are placed on owl after plug removal (C).

• No correction if vision is displaced using prisms (D)

Knudsen and Knudsen (1985)

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Vision guides plasticity

stimulus

stimulus

E. Knudsen, 1999

now owl responds normally to sound,

but makes 23 deg error to visual stim

After 42 days, the response to sound is also displaced

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Vision guides plasticity

stimulus

stimulus

E. Knudsen, 1999

now owl responds normally to sound,

but makes 23 deg error to visual stim

After 42 days, the response to sound is also displaced 42

When recording from neurons in Optic tectum, ITD from a neuron in the 0 degree azimuth part of the map is tuned to 0 degrees azimuth.

After 8 weeks with L23 prisms, a neuron in the zero degree part of map is now tuned to 50 microsecond ITD. (the map has become displaced)

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43 44

45 46

Spectral cues (used for vertical localization by humans) are shifted by modified

pinna (using ear molds).

Relearning sound localization with new ears.

Hofman PM, Van Riswick JG, Van Opstal AJ.

Nat Neurosci. 1998 Sep;1(5):417-21.

Plot shows monaural

sensitivity as function

of frequency and

sound elevation

(control listening

above, with modified

pinna shape (ear

mold)).

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Errors in elevation

estimation caused by

insertion of earmolds are

gradually corrected (over

39 days).

Removal of earmold results

in instantaneous recovery

of elevation accuracy.

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Lessons from Owls 1. Barn owls are “champions” at sound localization. Their auditory

system is specialized for this function both in terms of accuracy and the fact that it is a 2-D system that uses cues for both azimuth and elevation.

2. There are two parallel auditory systems in the owl: one specialized for analysis of ITD, the other for analysis of IID. These parallel pathways are specialized. For for encoding and preserving time one for encoding and preserving amplitude.

3. Combined in the midbrain, the owl generates an computational map of auditory space. (Computational: does not exist in the periphery)

4. ITD pathway generates a place map using delay-line + coincidence detectors. The place map was predicted by L. Jeffress (1948).

5. Alignment of the auditory map with the visual map in the optic tectum is plastic. In young owls it can be re-aligned by early experience.

6. Realignment of the map requires re-wiring of the neurons in the optic tectum by growth of dendrites and formation of new synapses.

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THE END