Plasticity in sensory systems

Jan Schnupp on the monocycle

Activity and size of auditory

cortex…

Schneider et al. Nat. Neurosci. 2003

…Are correlated…

…and correlated with musical abilities

Is musical practice increasing the size of auditory cortex, or do

people with large auditory cortex become musicians?

What do we learn when we learn a new skill?

Nat. Neurosci. 2006

Human psychoacoustical performance

Frequency differencesFrequency differencesPressure ratio between softest and loudest sounds…

Pressure ratio between softest and loudest sounds…

Hair motion at absolute threshold…Hair motion at absolute threshold…

Learning protocol

Perceptual learning

• Partially non-specific– Playing tetris improves frequency

discrimination

• Partially due to passive exposure

• But also to some extent requires active task performance

Animal models of auditory plasticity

• Classical conditioning– Fear conditioning: associating a sound with a

foot shock

• Environmental enrichment and relatives– Manipulating the environment can have both

beneficial and disruptive effects on the auditory system

• Spatial hearing

Nat. Rev. Neurosci. 2004

Fear conditioning…

…changes cortical neurons

Brain Research 2007

Environmental enrichment…

Environmental enrichment…

Environmental enrichment…

Plasticity in auditory enriched environments

Auditory plasticity requires stimuli but not interaction

Just noticeable differences in azimuthat the center, tone stimuli

timeam

plitu

de

Interaural Time Differences (ITDs)

Interaural Level Differences (ILDs)

Binaural Cues for Localising Sounds in Space

Interaural Time Difference (ITD) Cues

ITD

ITDs are powerful cues to sound source direction, but they are ambiguous (“cones of confusion”)ITDs are powerful cues to sound source direction, but they are ambiguous (“cones of confusion”)

Binaural disparities in humans

ITDITD ILDILD

Disambiguating the cone of confusion

• Sounds on the median plane (azimuth 0, different elevations) have zero binaural disparities

• This is a special case of the cone of confusion

• Nevertheless, humans and other animals can determine the elevation of a sound source

Spectral information about space

The barn owl…

Binaural Cues in the Barn Owl

Barn owls have highly asymmetric outer ears, with one ear pointing up, the other down. Consequently, at high frequencies, barn owl ILDs vary with elevation, rather than with azimuth (D). Consequently ITD and ILD cues together form a grid specifying azimuth and elevation respectively.

Phase locking at highfrequencies in the barn owl

C. Köppl, 1997

Processing of Interaural Time Differences

Interaural time difference

MS

O n

euro

n re

spon

s e

Sound on the ipsilateral side

Contra- lateral side

Medial superior olive

To the Inferior Colliculus

Preservation of Time Cues in AVCN

• Auditory Nerve Fibers connect to spherical and globular bushy cells in the antero-ventral cochlear nucleus (AVCN) via large, fast and secure synapses known as “endbulbs of Held”.

• Phase locking in bushy cells is even more precise than in the afferent nerve fibers.

• Bushy cells project to the superior olivary complex.

• Auditory Nerve Fibers connect to spherical and globular bushy cells in the antero-ventral cochlear nucleus (AVCN) via large, fast and secure synapses known as “endbulbs of Held”.

• Phase locking in bushy cells is even more precise than in the afferent nerve fibers.

• Bushy cells project to the superior olivary complex.

sphericalbushy

cell

sphericalbushy

cell

endbulbof Held

endbulbof Held

VIII nervefiber

VIII nervefiber

The coincidence detection model of Jeffress The coincidence detection model of Jeffress (1948) is the widely accepted model for low-(1948) is the widely accepted model for low-

frequency sound frequency sound localisationlocalisation

Res

pons

e

Interaural Time Difference0

Res

pons

e

Interaural Time Difference0

Window

SemicircularCanals

Left Ear Right EarCochlear Nucleus

MSO

0 s Time Delay

0 s

0 s Time Delay

Auditory Nerve ActivityLarge calyx synaptic ending

Cochlear Nucleus

Window

SemicircularCanals

Left Ear Right EarCochlear Nucleus

MSO

300 s Time Delay

300 s

Arrives at left ear 300 s later than at the right

Coincident spikes

Auditory Nerve ActivityLarge calyx synaptic ending

Cochlear Nucleus

Window

SemicircularCanals

Left Ear Right EarCochlear Nucleus

MSO

300 s Time Delay 0 s Time Delay

0 s300 s

0 s Time DelayArrives at left ear 300 s later than at the right

Coincident spikes

Auditory Nerve ActivityLarge calyx synaptic ending

Cochlear Nucleus

Interaural Phase Sensitivity in the MSO to 1000 Hz

Yin and Chan (1988)

1 ms 1 ms

Processing of Interaural Level Differences

Interaural intensity difference

LS

O n

eur o

n r e

s po n

se

Sound on the ipsilateral side

Contralateralside

C > II > CLateral superior olive

To the Inferior Colliculus

The Calyx of Held

• MNTB relay neurons receive their input via very large calyx of Held synapses.

• These secure synapses would not be needed if the MNTB only fed into “ILD pathway” in the LSO.

• MNTB also provides precisely timed inhibition to MSO.

Caird and Klinke 1983Frequency (kHz)

0.125 0.12532 32

Sou

nd le

vel (

dB S

PL)

20 20

100100

Ipsilateral Contralateral

The Superior Olivary Nuclei – a Summary

• Most neurons in the MSO respond best to sounds that occur earlier in the contralateral ear.

• Most neurons in the LSO respond best to sounds that are louder in the ipsilateral ear.

• Space representation is crossed, and therefore LSO projects mostly contralaterally and MSO ipsilaterally.

MNTBMNTB

MSOMSO

LSOLSO

CNCN CNCN

Midline

Inhibitory ConnectionExcitatory Connection

ICIC ICIC

Spatial hearing is plastic

Plasticity in adults

Nat. Neurosci. 1998

New ears…

Sound localization by humans

-30 0 30

Sound localization by humans

Effect of modifying the ear

Learning the new ears

Knowing both ears

Plasticity of the space map

Knudsen, Nature 2002

Orientation responses to auditory and visual stimuli are congruent…

Auditory orientation response

Visual orientation response

Prisms that shift the visual scene

Auditory responses adapt to the visual shift

The brain of the barn owl

The ICC, ICX and the Superior Collicullus (Optic Tectum)

Point-to-point correspondence between ICX and OT

Neural correlate of the shift of auditory responses

Shift in ITD sensitivity occurs first in ICX

Axonal sprouting cause shift of ITD sensitivity in ICX

Axonal sprouting cause shift of ITD sensitivity in ICX

Time course of ITD shift

Cellular mechanisms of ITD shift

Anatomy of the instructive signal

Visual activity in ICX uncovered by removing inhibition in OT

Cellular mechanisms of ITD shift

NMDA receptors are present at the transition stage…

…but not when the shift is complete

Cellular mechanisms of ITD shift

GABA participates in the suppression of the normal responses

Control

Bicuculline

Plasticity and age

Old animals cannot change

A sensitive period…

During the sensitive period, plasticity potential is very large

The normal map is robust and can be recovered at any age

Recovery of the normal map requires rich environment

Adult plasticity is possible after juvenile experience

Adult plasticity is possible after juvenile experience

Time course of adult adjustment