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Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

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Page 1: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Sensory Experience Alters Response Strength, Selectivity

and Temporal Processingof Auditory Cortex Neurons

Mike KilgardUniversity of Texas at Dallas

Page 2: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

• Pioneering experiments by Hubel and Wiesel, Merzenich, Weinberger, Greenough, and many others have shown that cortical circuits are highly adaptive.

• Neural plasticity is likely involved in perceptual learning, development, and recovery from brain injury.

Cochlea CortexTone Frequency

Act

ion

Pot

entia

ls

Page 3: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Time

Fre

quen

cy

15 Word Speech Stream >1045 possibilities

Page 4: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Techniques used to study how complex sounds alter cortical processing

Behavioral Nucleus Basalis Environmental Training Stimulation Enrichment

Page 5: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas
Page 6: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Environmental enrichment increases:• Brain weight

• Gene expression

• Cortical thickness

• Dendritic branching

• Acetylcholinesterase levels

• Oligodendrocyte to neuron ratio

• Number of synapses per neuron

What are the physiological consequences of these anatomical changes?

Page 7: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

20±10 vs. 75±20 μV 81±19 vs. 37±20 μV

0 50 100 150 200 250

Week 1

Am

plit

ud

e (

mV

)

Time (ms)0 50 100 150 200 250

Week 2

Time (ms)0 50 100 150 200 250

Week 5

Time (ms)

0 50 100 150 200 250

Week 12

Time (ms)

.10

.05

0

-.05

-.10

Red Group Enriched Blue Enriched

22 rats total

Journal of Neurophysiology, 2004

Page 8: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Environmental Enrichment

• Rapid

• Dramatic

• Reversible

• No critical period

Page 9: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Environmental Enrichment

• State dependent?• Other response properties change?• Consequences for speech processing?• What aspects of enrichment are required?

– Exercise– Social– Sensory

• Cellular mechanisms?

Page 10: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

High-density Microelectrode

Mapping

Page 11: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

1 2 4 8 16 320

20

40

60

80

BW10

BW20

BW30

BW40

CF

Frequency (kHz)

Inte

nsi

ty (

dB

SP

L)

A.

1 2 4 8 16 320

20

40

60

80

BW10

BW20

BW30

BW40

CF

B.

0 10 20 30 400

20

40

60

80

100C.

Time (ms)

Sp

ike

s/s

EnrichedStandard

First SpikeLatency

Peak Latency

End of Response

Enriched Housing

Standard Housing

Plasticity in Primary Auditory Cortex

Page 12: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

• 40% increase in response strength– 1.4 vs. 1.0 spikes per noise burst (p< 0.00001)

• 10% decrease in frequency bandwidth– 2.0 vs. 2.2 octaves at 40dB above threshold

(p< 0.05)

• 3 dB decrease in threshold– 17.2 vs. 20 dB (p< 0.001)

Enrichment effects persist under general anesthesia

n = 16 rats, 820 A1 sitesJournal of Neurophysiology, 2004

Page 13: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Time

Fre

quen

cy

Consequences for speech processing?

Page 14: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

-100 0 100 200 300 400 500 600 700 800 900

-60

-40

-20

0

20

40

60

Time (milliseconds)

Vo

ltag

e (

mic

rovo

lts)

200ms ISI

EnrichedStandard

200 ms Interstimulus Interval

Enrichment IncreasesPaired Pulse Depression

Page 15: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas
Page 16: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas
Page 17: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

50ms 100ms 200ms 500ms0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

Pai

red

Pu

lse

Ra

tio (

2nd

/1st

)

Interstimulus Interval (milliseconds)

EnrichedStandard

Page 18: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

• Response of Neurons at a Single Site to Repeated Tones

• Group Average

Page 19: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Enriched housing alters temporal processing

Decrease in best rate by 1.1 Hz in enriched rats7.8 vs. 6.7 Hz (p< 0.001)

Page 20: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Environmental Enrichment

• Rapid

• Dramatic

• Reversible

• No critical period

• Alters temporal processing

Why?

Page 21: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas
Page 22: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

WA

TE

Ra

nd

Exercise can cause:• A persistent firing pattern in the rat hippocampus,

known as theta-rhythm• Increased release of brain-derived neurotrophic factor

and other growth factors• Changes in gene regulation • Increased cell proliferation and neurogenesis in the

adult mouse dentate gyrus

No ef

fect

on

evok

ed p

oten

tials

Page 23: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

WA

TE

Ra

nd

No ef

fect

on

evok

ed p

oten

tials

Social Interactions can:• enhance some forms of learning• alter stress hormones• improve recovery from brain damage

Page 24: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Auditory Exposure Enriched Auditory Environment

Page 25: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Nucleus Basalis and Plasticity• Nucleus basalis neurons are activated by

any arousing stimuli.

• Cholinergic agonists and NB stimulation

increase plasticity.

• Cholinergic antagonists and NB lesions

prevent many forms of cortical

plasticity.No effect on

evoked potentials

Page 26: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Auditory Enrichment

• Rapid• Dramatic• Reversible• No critical period• Alters temporal processing• Not dependent on nucleus basalis• Not dependent on exercise or social interactions

Page 27: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Time

Fre

quen

cy

Page 28: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Enrichment Evoked Potentials - Cherie Percaccio

Enrichment A1 Experiments - Navzer Engineer

Acknowledgements:

For more information visit: www.utd.edu/~kilgard

Page 29: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Sash

Page 30: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

Spectrotemporal discharge patterns of A1 neurons to ‘sash’(n= 12 rats, 445 cortical sites)

Time (msec)

Sit

e

Nu

mb

er

kH

z S

pik

es p

er s

econ

d

High

Low

Page 31: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

050

100150

Spi

ke

Rat

e (H

z)

050

100150

Spi

ke

Rat

e (H

z)

050

100150

Spi

ke

Rat

e (H

z)F

requ

ency

(kH

z)

5 102025

Fre

quen

cy (

kHz)

5 102025

Fre

quen

cy (

kHz)

5 102025

050

100150

050

100150

050

100150

5 102025

5 102025

5 102025

A) 'back' E) 'back' - modified

B) 'pack' F) 'pack' - modified

C) 'sash' G) 'sash' - modified

50 100 150 200 250 300 350

50

100

150

Time (ms)

Spi

ke

Rat

e (H

z)

pack

backa sh

D) Neural responses to normal speech

50 100 150 200 250 300 350

50

100

150

Time (ms)

ba

p as a

ck

cksh

H) Neural responses to modified speech

Page 32: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

0 100 200 300 400 500 600 700 800 900-150

-100

-50

0

50

100

150

Time (milliseconds)

Vol

tage

(m

icro

volts

)

Individual Rat

0 100 200 300 400 500 600 700 800 900-75

-50

-25

0

25

50

75

Time (milliseconds)

Vol

tage

(m

icro

volts

)

Mean of Five Rats

BeforeDuringAfter

BeforeDuringAfter

Page 33: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas

0 100 200 300 400 500 600 700 800 900-150-100-50

050

100150

Time (milliseconds)

Vol

tage

(m

icro

volts

)

Individual Rat

0 100 200 300 400 500 600 700 800 900-75-50-25

0255075

Time (milliseconds)

Vol

tage

(m

icro

volts

)

Mean of Five Rats

BeforeDuringAfter

BeforeDuringAfter

Page 34: Sensory Experience Alters Response Strength, Selectivity and Temporal Processing of Auditory Cortex Neurons Mike Kilgard University of Texas at Dallas