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.
Action Potentials
• Neural plasticity is likely involved in
perceptual learning, development, and
recovery from brain injury.
Tone Frequency
Cochlea
Cortex
Frequency 
Time 
15 Word Speech Stream >1045 possibilities
Techniques used to study how
complex sounds alter cortical processing
Behavioral
Training
Nucleus Basalis
Stimulation
Environmental
Enrichment
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?
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
Journal of Neurophysiology, 2004
Environmental Enrichment
•
•
•
•
Rapid
Dramatic
Reversible
No critical period
Environmental Enrichment
•
•
•
•
State dependent?
Other response properties change?
Consequences for speech processing?
What aspects of enrichment are required?
– Exercise
– Social
– Sensory
• Cellular mechanisms?
High-density
Microelectrode
Mapping
Plasticity in Primary Auditory Cortex
B.
80
60
60
C.
80
BW40
BW40
40
BW30
BW30
40
BW20
BW20
20
BW10
BW10
20
1
2
4
8
16
60
First
Spike
Latency
40
20
End of Response
CF
CF
0
Enriched
Standard
100 Peak Latency
Spikes/s
Intensity (dB SPL)
A.
80
0
32
1
2
4
8
16
32
Frequency (kHz)
Enriched
Housing
Standard
Housing
0
0
10
20
30
Time (ms)
40
Enrichment effects persist under general anesthesia
• 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)
n = 16 rats, 820 A1 sites
Journal of Neurophysiology, 2004
Frequency 
Consequences for speech processing?
Time 
200ms ISI
200 ms Interstimulus
Interval
Enriched
Standard
60
Enrichment Increases
Paired Pulse Depression
40
Voltage (microvolts)
20
0
-20
-40
-60
-100
0
100
200
300
400
500
Time (milliseconds)
600
700
800
900
1
Paired Pulse Ratio (2nd/1st)
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
Enriched
Standard
0
50ms 100ms 200ms
500ms
Interstimulus Interval (milliseconds)
• Response of Neurons at a Single Site to Repeated Tones
• Group Average
Enriched housing alters temporal processing
Decrease in best rate by 1.1 Hz in enriched rats
7.8 vs. 6.7 Hz (p< 0.001)
Environmental Enrichment
•
•
•
•
•
Rapid
Dramatic
Reversible
No critical period
Alters temporal processing
Why?
Exercise can cause:
and
WATER
• 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
Social Interactions can:
and
WATER
• enhance some forms of learning
• alter stress hormones
• improve recovery from brain damage
Auditory Exposure
Enriched Auditory Environment
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
Auditory Enrichment
•
•
•
•
•
•
•
Rapid
Dramatic
Reversible
No critical period
Alters temporal processing
Not dependent on nucleus basalis
Not dependent on exercise or social interactions
Time 
Frequency 
Acknowledgements:
Enrichment Evoked Potentials - Cherie Percaccio
Enrichment A1 Experiments
- Navzer Engineer
For more information visit: www.utd.edu/~kilgard
Sash
kHz
Spikes per second
Site Number
High
Low
Time (msec)
Spectrotemporal discharge patterns of A1 neurons to ‘sash’
(n= 12 rats, 445 cortical sites)
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)
Individual Rat
Voltage (microvolts)
150
Before
During
After
100
50
0
-50
-100
-150
0
100
200
300 400 500 600
Time (milliseconds)
700
800
900
Mean of Five Rats
Voltage (microvolts)
75
Before
During
After
50
25
0
-25
-50
-75
0
100
200
300 400 500 600
Time (milliseconds)
700
800
900
Voltage (microvolts)
150
100
50
0
-50
-100
-150
Voltage (microvolts)
Individual Rat
75
50
25
0
-25
-50
-75
Before
During
After
0 100 200 300 400 500 600 700 800 900
Time (milliseconds)
Before
Mean of Five Rats
During
After
0 100 200 300 400 500 600 700 800 900
Time (milliseconds)