Sensory Experience
and Cortical Plasticity
Michael P. Kilgard
University of Texas at Dallas
Environmental
Enrichment
Red Group Enriched
Blue Enriched
Amplitude (mV)
.10
Week 1
Week 2
Week 5
Week 12
.05
0
-.05
-.10
0
50 100 150 200 250
Time (ms)
22 rats total
0
50 100 150 200 250
Time (ms)
0
50 100 150 200 250
Time (ms)
20±10 vs. 75±20 μV
0
50 100 150 200 250
Time (ms)
81±19 vs. 37±20 μV
A1 Enrichment Effects
- after 2 months
A.
Intensity (dB SPL)
• 40% increase in response strength
– 1.4 vs. 1.0 spikes per noise burst (p< 0.0001)
• 10% decrease in frequency bandwidth
Intensity (dB SPL)
Intensity (dB SPL)
A.
80
40
20
0
1
80
2
4
8
16
32
Standard
60
40
20
0
1
2
4
8
16
32
Frequency (kHz)
60
40
C.
Stronger, More Selective, and More Sensitive
100
1
2
4
8
16
32
B.
Spikes/s
20
Frequency (kHz)
Intensity (dB SPL)
60
B.
• Three decibel decrease in threshold
0
Enriched
Frequency (kHz)
– 2.0 vs. 2.2 octaves at 40dB above threshold (p< 0.05)
– 17 vs. 20 dB ms (p< 0.001)
80
50
80
0
60
0
10
20
30
40
Time (ms)
40
Environmental Enrichment Improves Response Strength, Threshold, Selectivity, and Latency of Auditory Cortex Neurons
Engineer ND, Percaccio CR, Pandya PK, Moucha R, Rathbun DL, Kilgard MP. Journal of Neurophysiology, 20
2004.
0
1
2
N = 16 rats, 820 sites
4
8
16
Frequency (kHz)
32
High
Low
Cochlea
Cortex
Cortical Map Plasticity
High
Low
Cochlea
Cortex
High-density microelectrode mapping technique
Best Frequency
Nucleus Basalis Activity Enables Cortical Map Reorganization
M.P. Kilgard, M.M. Merzenich, Science 279(5357): 1714-1718, 1998. download file
Nucleus Basalis Stimulation
Generates Frequency-Specific
Map Plasticity
Tone Frequency - kHz
N = 20 rats; 1,060 A1 sites
Differences between A1 and Posterior Auditory Field – submitted
Intensity (dB)
70
40
50
30
10
Plasticity in Posterior Auditory Field
20
• High2 frequency
map8 expansion
, p<0.01
4
16
32
C
Difference in PAF Percent after 19 kHz Paired
20
70
Intensity (dB)
0
10
50
0
30
-10
10
2
4
8
16
32
-20
Tone Frequency (kHz)
• Decreased bandwidth (30 dB above threshold)
– 3.0 vs. 3.6 octaves, p<0.001
• Shorter time to peak
– 56 vs. 73 ms, p<.01
N = 12 rats; 396 PAF sites
Manuscript in preparation
Typical Response of A1 Neurons to Tone Trains
Temporal Processing
• After Pairing NB Stimulation with 15 Hz Tone Trains
• After Pairing NB Stimulation with 5 Hz Tone Trains
Plasticity of Temporal
Information Processing
in the Primary Auditory Cortex
M.P. Kilgard, M.M. Merzenich
Nature Neuroscience
1(8): 727-731, 1998
download file
N = 15 rats, 720 sites
Frequency Bandwidth Plasticity
N = 52 rats; 2,616 sites
Stimulus Paired with NB Activation Determines
Degree and Direction of Receptive Field Plasticity
Frequency Bandwidth is Shaped by
Spatial and Temporal Stimulus Features
50 %
100%
Leads to
Larger RF’s
15%
Tone Probability
Temporal
Modulation
Spatial
Variability
Leads to
Smaller RF’s
0
5
10
15
Modulation Rate (pps)
Sensory Input Directs Spatial and Temporal Plasticity in Primary Auditory Cortex
M.P. Kilgard, P.K. Pandya, J.L. Vazquez, Gehi, A., C.E. Schreiner, M.M. Merzenich
Journal of Neurophysiology, 86: 339-353, 2001. download file
How do neural networks learn
to represent complex sounds?
• Spectrotemporal Sequences
High Tone
(12 kHz)
Low Tone
(5 kHz)
100ms
Noise Burst
20ms
High Tone
(12 kHz)
Low Tone
(5 kHz)
Noise Burst
Paired w/ NB
stimulation
100ms
20ms
Unpaired
background
sounds
Noise Burst
0
100
200
300
400ms
Spikes per Element
Number of Spikes
/ BF
rsed
rsed
sed
Context-Dependent Facilitation
ched
1.1
0.1
0.3
0.7
2.2
+42%
2
1.5
0.1
0.8
1
0
1.2
1
0.6
1.7
0.2
1.7
aded
aded
High Tone
(12 kHz)
Low Tone
(5 kHz)
Noise Burst
rsed
1.6
Spikes per Element
/ BF
rsed
1.3
100ms
20ms
0.1
0.7
0.5
0.1
1.3
0.4
2.5
+67%
2.7
+80%
0.3
Context-Dependent Facilitation - Group Data
• 58% of sites respond with more spikes to the noise
when preceded by the high and low tones, compared to
35% in naïve animals. (p< 0.01)
Noise Burst
High Tone
(12 kHz)
Low Tone
(5 kHz)
Noise Burst
Order Sensitive Plasticity in Adult Primary Auditory Cortex
M.P. Kilgard, M.M. Merzenich
Proceedings of the National Academy of Sciences
99: 3205-3209, 2002. download file
N = 13 rats, 261 sites
Schematic
Illustration
100ms
20ms
Context-Dependent Facilitation - Group Data
• 25% of sites respond with more spikes to the low tone
when preceded by the high tone, compared to 5% of sites in
naïve animals. (p< 0.005)
Low Tone
(5 kHz)
High Tone
(12 kHz)
Low Tone
(5 kHz)
Noise Burst
Order Sensitive Plasticity in Adult Primary Auditory Cortex
M.P. Kilgard, M.M. Merzenich
Proceedings of the National Academy of Sciences
99: 3205-3209, 2002. download file
N = 13 rats, 261 sites
Schematic
Illustration
100ms
20ms
Context-Dependent Facilitation - Group Data
• 10% of sites respond with more spikes to the high tone
when preceded by the low tone, compared to 13% of sites
in naïve animals.
High Tone
(12 kHz)
Low Tone
(5 kHz)
High Tone
(12 kHz)
Noise Burst
Order Sensitive Plasticity in Adult Primary Auditory Cortex
M.P. Kilgard, M.M. Merzenich
Proceedings of the National Academy of Sciences
99: 3205-3209, 2002. download file
N = 13 rats, 261 sites
Schematic
Illustration
100ms
20ms
Operant Training
Task
Target stimulus
(CS+)
Add first
distractor
(CS-1)
None
A) Sequence detection
H L
B) Frequency
discrimination
H H
H
H L
N
H H
H
D) Sequence element
discrimination
H L
N
H
E) Triplet distractorNoise first
H L
N
N N
Frequency (kHz)
L
None
None
None
None
L L
L
L
N
N
N L
N N
N
N
L L
L
None
F) Reverse Order
H L
Add third
distractor
(CS-3)
N
L L
C) Triplet distractorHigh first
Add second
distractor
(CS-2)
H
Time (ms)
Time (months)
H H
H
None
Map
Auditory Cortex
Discrimination Performance
Differential Plasticity Effects
How do cortical neurons learn to
represent speech sounds?
Sash
kHz
‘SASH’ Group - Spectrotemporal discharge patterns of A1 neurons to ‘sash’ vocalization (n= 5 rats)
16kHz @50dB:
35 %  1.9
55 %  5.3
(p<0.0005)
Sensory Experience Controls:
• Response Strength
• Cortical Topography
• Receptive Field Size
• Maximum Following Rate
• Synchronization
• Spectrotemporal Selectivity
E)
Frequency
(kHz)
'back'
25
20
10
5
25
20
10
5
Spike
Rate (Hz)
A)
150
100
50
0
150
100
50
0
Spike
Frequency
Rate (Hz)
(kHz)
B)
'pack'
Frequency
Spike
Rate (Hz)
(kHz)
Spike
Rate (Hz)
D)
F)
25
20
10
5
25
20
10
5
150
100
50
0
150
100
50
0
C)
'back' - modified
'sash'
'pack' - modified
G)
25
20
10
5
25
20
10
5
150
100
50
0
150
100
50
0
'sash' - modified
Neural responses to normal speech H) Neural responses to modified speech
150
100
50
back
150
a
sh
pack
100
50
50 100 150 200 250 300 350
Time (ms)
ba
s
p a
ck
a
sh
ck
50 100 150 200 250 300 350
Time (ms)
Activity from a single A1 neuron
recorded in an awake rat
in response to normal and enhanced
human speech sounds
External World
-Sensory Input
Neural
Activity
- Internal
Representation
Behavioral
Relevance
Plasticity Rules
- Educated Guess
Neural
Plasticity
- Learning and
Memory
Behavioral
Change
Acknowledgements:
Training Experiments
- Navzer Engineer
Amanda Puckett
and
Crystal Novitski
Enrichment Experiments
- Navzer Engineer
and
Cherie Percaccio
Receptive Field Plasticity
- Pritesh Pandya
Synchrony Experiments
- Jessica Vazquez
FM Experiments
- Raluca Moucha
Speech Experiments
- Pritesh Pandya