michael p. kilgard sensory experience and cortical plasticity university of texas at dallas

Michael P. Kilgard

Sensory Experience and Cortical Plasticity

University of Texas at Dallas

Cortical plasticity depends upon:

• Sensory experience

• Behavioral relevance

The Cholinergic Basal Forebrain Provides a Diffuse Neuromodulatory Input to the Cortex

Nucleus Basalis

Exploring the Principles of Cortical Plasticity using:• Systematic Variation of Sensory Experience

• Nucleus Basalis Stimulation to

Gate Cortical Plasticity

Experienceor Instinct

Connectivity & Dynamics

Plasticity

Neural Representation

Importance

External world

• NB stimulation is paired with a sound several hundred times per day for ~20 days.

• Pairing occurs in awake unrestrained adult rats.

• Stimulation evokes no behavioral response.

• Stimulation efficacy is monitored with EEG.

Extracellular Recordings

Detailed Reconstruction of the Distributed Cortical Response

Best Frequency

Science, 1998

Tone Frequency - kHz

Nucleus Basalis Stimulation Generates Map Plasticity that is Specific to the Paired Tone

N = 20 rats; 1,060 A1 sites

Nature Neuroscience, 1998

Temporal Plasticity is Specific to the

Paired Repetition Rate

N = 15 rats, 720 sites

2 4 6 8 10 12 14 16 18 200

0.2

0.4

0.6

0.8

1

1.2

Repetition Rate (pulses/second)

Nor

mal

ized

Spi

ke R

ate

Control 15pps 9 kHz 15pps Seven Carriers

0 5 10 15 200

20

40

60

80

100

Best Repetition Rate(pulses/second)

Per

cent

of S

ites

A.

B.

Journal of Neurophysiology, 2001

Carrier frequency variability prevented map expansion and allowed temporal plasticity.


Stimulus Paired with NB Activation Determines

Degree and Direction of Receptive Field Plasticity

Frequency Bandwidth Plasticity N = 52 rats; 2,616 sites

Frequency Bandwidth is Shaped by Spatial and Temporal Stimulus Features

Modulation Rate (pps)0 5 10 15

Ton

e P

rob

abil

ity

15%

50 %

10

0%

Journal of Neurophysiology, 2001

Neuron 1

Inputs to Neuron A

Neuron 2

Receptive Field Overlap

Neuron A Neuron B

Inputs to Neuron B

Spike synchronization and RF overlap are correlated.

Brosch and Schreiner, 1999

After Map Expansion: ~85% shared inputs

After Sharper Frequency Tuning: ~25% shared inputs

What is the effect of cortical plasticity on spike synchonization?

Before plasticity: ~50% shared inputsBefore Plasticity: ~50% shared inputs

-50 -40 -30 -20 -10 0 10 20 30 40 500

200

400

600

800

1000

1200N

um

ber

of

Inte

rval

s

Interval (msec)

Cross-correlation: TC 025C1.MAT x TC025C2.MAT

Cross-correlationShift PredictorCorrelation strength

= correlation peak in normalized cross-correlation

histogram

Correlation width = width at half height

of correlation peak

Experience-Dependent Changes in Cortical Synchronization

• Map expansion sharpened synchronization– 15pps 9kHz tone trains

50% increase in cross-correlation height (p<0.0001)

17% decrease in cross-correlation width (p<0.01)

• Bandwidth narrowing smeared synchronization– Two different tone frequencies

50% decrease in cross-correlation height (p<0.0001)

22% increase in cross-correlation width (p<0.001)

• Intermediate stimuli caused no change in synchronization– 15pps tone trains with several different carrier frequencies

No change in cross-correlation height or width

N = 23 rats; 1,129 sites; 404 pairs

Experience-Dependent Changes in Cortical Synchronization (con’t)

• Broadband ripple stimulus sharpened synchronization– Sinusoidal power spectrum (one cycle / 6kHz )

54% increase in cross-correlation height (p<0.0001)

27% decrease in cross-correlation width (p<0.01)

N = 9 rats; 310 sites; 147 pairs

Pairing NB stimulation with aspectrotemporal sequence sharpens

response discharge coherence.

0 10 20 100 110 120 200 210 220 230

-10

0

10

20

30

0

10

20

30

0

10

20

30

40

0

10

20

30

40P

erce

nt o

f Site

s

Time (ms)

CF < 3.2 kHz

CF 3.2-7.75 kHz

CF 7.75-18.6 kHz

CF >18.6 kHz

Sharpened Cortical Response to High-Low-Noise Sequence

// //

// //

Naive After HLN Difference

5 10 15 20 25 300

10

20

30

40

Time to Peak Response (ms)

Per

cent

of S

ites

A)

B)

0 10 20 100 110 120 200 210 220 230-10

0

10

20

30

0

10

20

30

0

10

20

30

40

0

10

20

30

40P

erce

nt o

f Site

s

Time (ms)

CF < 3.2 kHz

CF 3.2-7.75 kHz

CF 7.75-18.6 kHz

CF >18.6 kHz


// //

// //

Naive After HLN Difference

5 10 15 20 25 300

10

20

30

40


Per

cent

of S

ites

A)

B)

Peak Latency: 15.2 vs. 18.2 ms (p< 0.00001)

Difference

NaiveAfter HLN



Time (ms)

Spi

kes

per

Sec

ond


0 10 20 100 110 120 200 210 220 230-10

0

10

20

30

0

10

20

30

0

10

20

30

40

0

10

20

30

40

Spi

kes

per

seco

nd

Time (ms)

CF < 3.2 kHz

CF 3.2-7.75 kHz

CF 7.75-18.6 kHz

CF >18.6 kHz


// //

// //Naive After HLN Difference

5 10 15 20 25 300

20

40

60

Minimum Latency (ms)

Per

cent

of

Si te

s

5 10 15 20 25 300

20

40

60


Per

cent

of

Si te

s

A) B)

C)

Increased Population Discharge Coherence

1.1 0.1 2.2+42%

1 0 1.2

1 0.6 1.7

1.5 0.1 0.8

0.3 0.7 2

0.2 1.7

1.3 1.6

Spikes per Element

Stretched

Compressed

Tones Reversed

Degraded

Degraded

Paired w/ BF

Sequence Reversed

High Tone Low Tone Noise Burst

0.1 0.7 2.5+67%

0.2 0.4 2.1

0.1 0.6 2.8+87%

1.3 0.4 0.3

0.5 0.1 2.7+80%

0.6 2.3+53%

0.2 1.5

Spikes per Element

Stretched

Compressed

Tones Reversed

Degraded

Degraded

Paired w/ BF

Sequence Reversed

0 100 200 300 400

1.2 1.4+195%

2.1+35%

1.1 0-100%

1.6

1 1.3+174%

2.6+67%

1.6 1+111%

1

0.4 0.9 2.4+54%

0.5 1.6

1.2 2.1+35%

Spikes per Element

Time (ms)

Stretched

Compressed

Tones Reversed

Degraded

Degraded

Paired w/ BF

Sequence Reversed

A)

B)

C)

Context-Dependent Facilitation

• 5% of sites in naïve animals respond with more spikes to the 5 kHz tone when preceded by the 12 kHz tone, compared to 25% after sequence pairing. (p< 0.005)

• 35% of sites in naïve animals respond with more spikes to the noise when preceded by the high and low tones, compared to 58% after sequence pairing. (p< 0.01)

• 13% of sites in naïve animals respond with more spikes to the 12 kHz tone when preceded by the 5 kHz tone, compared to 10% after sequence pairing.

Context-Dependent Facilitation - Group Data


Sensory Experience Controls:

• Cortical Topography

• Receptive Field Size

• Maximum Following Rate

• Spectrotemporal Selectivity

• Synchronization

• 55% increase in response strength– 1.4 vs. 0.9 spikes per noise burst (p< 0.0001)

• 22% decrease in frequency bandwidth– 1.8 vs. 2.2 octaves at 30dB above threshold (p< 0.0001)

• One millisecond decrease in minimum latency– 15.8 vs. 16.8 ms (p< 0.005)

• Two decibel decrease in threshold– 17 vs. 19 dB ms (p< 0.01)

• Increased synchronization– 13% increase in cross-correlation height (p< 0.01)

Enrichment Effects




Plasticity


Importance

External world

Rules of Cortical Plasticity



Plasticity


Importance

External world



Plasticity

Behavioral Change


Importance

External world

Map BW LatencyEnd of

ResponseSpontaneous

ActivityTone

ResponseRipple

Response

One Frequency 0 0 0 0

Two Frequencies 0 0 0

MultipleFrequencies

0 0 0

Spectral Ripple 0

Spectral Stimuli

Map BW LatencyEnd of

ResponseSpontaneous

ActivityTone

Response

MaximumFollowing

Rate

CombinationSensitivity

15 pps Tone Trains - 9kHz Carrier 0 0 0 0

15 pps Tone Trains - Multiple Carrier Frequencies

0 0 0 0 0


0 0 0

High-Low-NoiseSequence

0 0

Temporal Stimuli

Rules of Cortical PlasticityMap BW Latency

End ofResponse

SpontaneousActivity

ToneResponse

MaximumFollowing

Rate

CombinationSensitivity

One Frequency 0 0 0 0

Two Frequencies 0 0 0

MultipleFrequencies

0 0

Spectral Ripple

15 pps Tone Trains - 9kHz Carrier

0 0 0 0


0 0 0 0 0


0 0 0

High-Low-NoiseSequence

0 0

Behavioral Relevance

Neural Activity

- Internal Representation

External World-Sensory Input

Neural Plasticity- Learning and

Memory

Plasticity Rules- Educated Guess

RF Increase Increased Synchrony

Temporal Task: BF Pairing 15 pps, 9 kHz Tone

Width

RF Decrease Decreased Synchrony

Spectral Task: BF Pairing 2 Frequencies Randomly Interleaved

Width

RF Increase No Change in Synchrony

Temporal and Spectral Task: BF Pairing 15 pps Multiple Frequencies

Width

No Change in RF Increased Synchrony

Spectral-temporal Task: BF Pairing Moving Stimuli (FM’s)

Width

RF Decrease Increased Synchrony

Complex Spectral Task: BF Pairing Steady State High Density Ripple

Width

michael p. kilgard sensory experience and cortical plasticity university of texas at dallas

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